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Role of gastrointestinal microbiota in fish

Sukanta K Nayak

Laboratory of Fish Pathology, Department of Veterinary Medicine, College of Bioresorece Sciences, Nihon University, Kanagawa 252-8510, Japan

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Sukanta K Nayak,

Sukanta K Nayak

Laboratory of Fish Pathology, Department of Veterinary Medicine, College of Bioresorece Sciences, Nihon University, Kanagawa 252-8510, Japan

Search for more papers by this author

First published: 16 June 2010

https://doi.org/10.1111/j.1365-2109.2010.02546.x

Citations: 784

Correspondence: S K Nayak, Laboratory of Fish Pathology, Department of Veterinary Medicine, College of Bioresorece Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan. E. Mail: [email protected]

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Abstract

The gastrointestinal (GI) tract of an animal consists of a very complex and dynamic microbial ecosystem that is very important from a nutritional, physiological and pathological point of view. A wide range of microbes derived from the surrounding aquatic environment, soil/sediment and feed are found to colonize in the GI tract of fish. Among the microbial groups, bacteria (aerobic, facultative anaerobic and obligate aneraobic forms) are the principal colonizers in the GI tract of fish, and in some fish, yeasts are also reported. The common bacterial colonizers in the GI tract of freshwater and marine fish include Vibrio, Aeromonas, Flavobacterium, Plesiomonas, Pseudomonas, Enterobacteriaceae, Micrococcus, Acinetobacter, Clostridium, Fusarium and Bacteroides, which may vary from species to species as well as environmental conditions. Besides, several unknown bacteria belonging to Mycoplasma, Arthrobacter, Brochothrix, Jeotgailbacillus, Ochrobactrum, Psychrobacter and Sejongia species in the GI tract of different fish species have now been identified successfully using culture-independent techniques. Gnotobiotic and conventional studies indicate the involvement of GI microbiota in fish nutrition, epithelial development, immunity as well as disease outbreak. This review also highlights the need for manipulating the gut microbiota with useful beneficial microbes through probiotic, prebiotic and synbiotic concepts for better fish health management.

Introduction

The first observation on the occurrence of a gastrointestinal (GI) microorganism in any host was made by Leewenhock in 1674 (DoBell 1932). However, the comprehensive study of intestinal bacteria was initiated only after the discovery of Escherichia in the human GI tract, which laid the foundation of GI microbiota in other species. With the advent of the 20th century, the distribution of GI microbiota has been studied extensively in various animals for different purposes. The GI ‘microbiota’ usually refers to a very complex and dynamic microbial ecosystem that colonizes the GI tract of an animal. Furthermore, with the developments in molecular and biotechnological tools, this complex ecosystem is beginning to be unravelled in many species (Rastall 2004).

The mammalian GI tract contains an enormous variety of aerobic and anaerobic microbes that interact in its complex ecosystem (Eckburg, Bik, Bernstein, Purdom, Dethlefsen, Sargent, Gill, Nelson & Relman 2005; Nicholson, Holmes & Wilson 2005), but that of fish is believed to be simpler and less in number than that of endothermic animals (Trust & Sparrow 1974; Horsley 1977; Finegold, Suher & Mathisen 1983; Sakata 1990). Until the 1970s, a concrete report on the existence of a stable indigenous microbiota in many aquatic animals was not available (Savage 1977; Yoshimizu, Kimura & Sakai 1980; Ringø, Olsen, Mayhew & Myklebust 2003), but during the past few decades, substantial research has been carried out to characterize the GI microbiota in a wide range of fish species (Ringø, Strom & Tabachek 1995; Ringø & Gatesoupe 1998; Ringø, Lodemel, Myklebust, Kaino, Mayhew & Olsen 2001; Ward, Steven, Penn, Methe & Detrich III 2009). However, most of the earlier GI microbiota studies in fish have emphasized the microbial spoilage, environmental relationship (Horsley 1973), their enzymatic ability (Shcherbina & Kazlawlene 1971; Lindsay & Harris 1980), studies on nutritional aspects (Moriarty 1990), monitoring of the changes in farms (Allen, Austin & Colwell 1983) and antibiotic resistance (Ogbondeminu & Olayemi 1993).

The GI microbiota serve a variety of functions in the host and their importance in the nutrition and health of the host by promoting nutrient supply, preventing the colonization of infectious agents, energy homeostasis and maintenance of normal mucosal immunity is well documented in mammals (Xu, Bjursell, Himrod, Deng, Carmichael, Chiang, Hooper & Gordon 2003; Nicholson et al. 2005; Delzenne & Cani 2008). Although the presence of native GI microbiota in fish has been recognized, little is known about the bacterial communities and their establishment, diversity and most importantly their role in fish nutrition and health. Therefore, an attempt has been made to review the information available for a better understanding of the GI microbes and their possible functional roles in fish.

Development and establishment of GI microbiota of fish

The microbial colonization, establishment, composition and diversity in the GI tract of fish is a complex process and believed to be a reflection of the microbial composition of the rearing water, diet and their environment (Liston 1957; Geldreich & Clarke 1966; Nieto, Toranzo & Barja 1984; Buras, Duek, Niv, Hepher & Sandbank 1987; Ogbondeminu 1993; Korsnes, Nicolaisen, Skar, Nerland & Bergh 2006; Ringø, Sperstad, Myklebust, Refstie & Krogdahl 2006; Ringø, Sperstad, Myklebust, Mayhew & Olsen 2006; Fjellheim, Playfoot, Skjermo & Vadstein 2007). Two distinct groups, i.e. either allochthonous (transient) and autochthonous (adherent), are usually found in the GI tract of fish. The latter group of bacteria, by virtue of their ability to tolerate the low pH in gastric juices and resistance to the actions of bile acids, only succeeded in colonizing in the epithelial surface of the stomach, small and large intestine (Savage 1989). These bacteria can firmly attach to the intestinal mucosa to become the autochthonous microbiota of the host (Yoshimizu, Kimura & Sakai 1976; Onarheim & Raa 1990; Sakata 1990; Onarheim, Wiik, Burghardt & Stackebradt 1994). The other group of bacteria is present transiently in the GI tract because they are not able to colonize the mucus layer and/or the epithelial surface (Ringø & Birkbeck 1999). They either lack this ability entirely or are so ineffective at it that they are outcompeted by other bacteria in the mucus/epithelium.

The initial colonization process is very complex at larval and fry and mostly depend on the fish type, nutrients/food and surrounding conditions (Bignell 1984; Voveriene, Mickeniene & Syvokiene 2002). The total bacterial load at the larval stage is low (approximately 10² CFU larva⁻¹) before active feeding (Munro, Barbour & Birkbeck 1994; Verner-Jeffreys, Shields, Bricknell & Birkbeck 2003; Reid, Treasurer, Adam & Birkbeck 2009), and this initial load is mostly derived from the water by larvae to maintain osmotic balance (Tytler & Blaxter 1988; Reitan, Natvik & Vadstein 1998). However, the number increases rapidly (>10⁵ CFU larva⁻¹) once the larvae start to feed (Munro, Birkbeck & Barbour 1993; Munro et al. 1994).

Furthermore, the microbial composition and density also vary in different regions of the GI tract of fish depending on the physico-chemical conditions of gut. In fish, a progressive increase in culturable bacterial levels from the stomach to the posterior intestine is often reported (Trust & Sparrow 1974; MacDonald, Stark & Austin 1986; Molinari, Scoaris, Pedroso, Bittencourt, Nakamura, Ueda-Nakamura, Abreu Filho & Dias Filho 2003). Molinari et al. (2003) recorded higher viable bacteria in both the anterior and the posterior gut than in the stomach of semi-intensively cultured Oreochromis niloticus. However, with the successful application of modern non-culturable techniques, the composition of bacteria in the GI tract and their percentage may vary with respect to fish. Recently, Navarrete, Espejo and Romero (2009) recorded the average bacterial density to be 1 × 10⁷, 8 × 10⁶ and 5 × 10⁷ bacteria g⁻¹ in the stomach, pyloric caeca and intestine, respectively, in Salmo salar using epifluorescence microscopy.

Factors affecting the establishment of GI microbiota

A series of exogenous and endogenous factors can affect the establishment and nature of the microbial composition in the GI tract of fish. The developmental stage of fish (Bell, Hoskins & Hodgkiss 1971; Sugita, Enomoto & Deguchi 1982; Sugita, Tokuyama & Deguchi 1985), gut structure (Sera, Ishida & Kadota 1974; Sugita et al. 1985), the surrounding environment like ambient water temperature (Lesel & Peringer 1981; Sugita, Oshima, Tamuar & Deguchi 1989), rearing and farming conditions (Trust & Sparrow 1974; Trust 1975; Yoshimizu & Kimura 1976; Horsley 1977; Sugita, Isida, Deguchi & Kadota 1982; Ringø & Strom 1994) are very critical factors that affect the initial colonization and the subsequent establishment process. Besides, stress factors can significantly affect the GI microbiota (Lesel & Sechet 1982). When different types of chemicals, antibiotics, pollutants like pesticides, herbicides and insecticides enter into the digestive tract of an aquatic animal, they can drastically affect the composition of dominant GI microbiota and may lead to the elimination of individual species from the whole microbial community (Austin & Al-Zahrani 1988; Sugita, Fukumoto, Koyama & Deguchi 1988; Sugita et al. 1989; Syvokiene & Mickeniene 2002; Bakke-McKellep, Koppang, Gunnes, Sanden, Hemre, Landsverk & Krogdahl 2007; Mickeniene & Syvokiene 2008; Navarrete, Mardones, Opazo, Espejo & Romero 2008).

Feed and feeding conditions considerably influence the composition of GI microbiota of fish (Campbell & Buswell 1983; Sugita, Tsunohara, Fukumoto & Deguchi 1987; Syvokiene 1989; Onarheim & Raa 1990; Ringø 1993; Ringø & Olsen 1999; Uchii, Matsui, Yonekura, Tani, Kenzaka, Nasu & Kawabata 2006; Ringø, Sperstad, Myklebust, Refstie et al. 2006; Martin-Antonio, Manchado, Infante, Zerolo, Labella, Alonso & Borrego 2007), and during the larval stage, the gut microbial flora has been found to change rapidly with respect to feed (Brunvold, Sandaa, Mikkelsen, Welde, Bleie & Bergh 2007; Reid et al. 2009). A positive correlation of capelin roe diet with Enterobacteriaceae in the GI microbiota of wild charr irrespective of freshwater and seawater maintenance was recorded by Ringø and Strom (1994). However, they have recorded the predominance of Aeromonas in freshwater and the Vibrio species under marine conditions from wild catch charr fed with a commercial diet. Recently, Ringø, Sperstad, Myklebust, Mayhew et al. (2006) recorded the variation in GI microbiota with respect to the diet. Ringø and colleagues observed the dominance of Gram-positive bacteria belonging to Brochothrix and Carnobacterium species in the GI tract of Gadus morhua fed with fish meal, while Psychrobacter species and Psychrobacter glacincola, Chryseobacterium and Carnobacterium species dominated the GI tract when fed with bio-processed soybean meal and standard soybean respectively.

Furthermore, the seasonal and day-to-day fluctuations in GI bacteria in different fish species have also been recorded (Sugita et al. 1987; MacMillan & Santucci 1990; Spanggaard, Huber, Nielsen, Nielsen, Appel & Gram 2000; Al-Harbi & Uddin 2004; Hagi, Tanaka, Iwamura & Hoshino 2004). Variations in the total viable GI bacterial counts from 1.6 × 10⁶ to 5.1 × 10⁷ CFU g⁻¹ intestine in summer, 3.1 × 10⁸ to 1.3 × 10⁹ CFU g⁻¹ intestine in autumn and 8.9 × 10⁵ to 1.3 × 10⁷ CFU g⁻¹ intestine in winter were recorded in hybrid tilapia (O. niloticus×Oreochromis aureus) (Al-Harbi & Uddin 2004). Similarly, MacMillan and Santucci (1990) reported seasonal variations among the bacterial species belonging to Escherichia coli, Klebsiella, Pseudomonas, Plesiomonas, Shigelloides, Streptococcus and Moraxella species in farm-raised Ictalurus punctatus. In a yearlong study on the changes in lactic acid bacteria (LAB) composition, Hagi et al. (2004) found the predominance of Lactococcus lactis in summer (water temperature >20 °C) and Lactococcus raffinolactis in winter (water temperature range 4–10 °C) in the GI tract of Cyprinus carpio. Inter-individual variation and highest daily fluctuation of Bacteroides species in the GI tract of fish like C. carpio have also been observed (Asfie, Yoshijima & Sugita 2003).

Microbial composition in the GI tract of fish

The GI tract is a favourable ecologic niche for microorganisms, and like any other animals, a wide range of microbes colonize in the GI tract of fish (Skrodenyte-Arbaciauskiene 2007). However, information on the type of bacterial composition in the GI tract of fish is often controversial (Izvekova & Lapteva 2004). Most of the earlier studies of fish GI microbiota have been derived from the homogenates of intestinal content and/or faecal materials using culture-based techniques using selective or non-selective isolation media, followed by phenotypic characterization using a series of conventional morphological and biochemical assays (Horsley 1977; Sakata, Sugita, Mitsuoka, Kakimoto & Kadota 1981; Sugita, Oshima, Tamura & Deguchi 1983; Sakata 1989, 1990; Sugita et al. 1989; Cahill 1990; Onarheim & Raa 1990; Zaman & Leong 1994; Ringøet al. 1995; Sivakami, Premkishore & Chandran 1996). However, conventional methods are often time consuming and lack accuracy (Asfie et al. 2003) and sensitivity in characterizing certain fastidious and obligate anaerobes that require special culture conditions. Therefore, culture-based study of GI microbiota of any animal often leads to a very uncertain picture of the total microbial community residing inside the tract.

Nowadays, several novel molecular technologies are being increasingly used for the analysis of microbes present in the complex GI ecosystem of animals. Molecular techniques based on genotypic fingerprinting techniques such as colony hybridization with nucleic acid probes, pulsed field gel electrophoresis, ribotyping, polymerase chain reaction (PCR), random amplified polymorphic DNA, multiplex-PCR, arbitrary primed-PCR and triplet arbitrary primed-PCR, denaturing gradient gel electrophoresis (DGGE), temporal temperature gradient gel electrophoresis, fluorescence in situ hybridization (FISH) and also electron microscopy have been used to study and characterize the microbes in the GI tracts of many animals including fish (Spanggaard et al. 2000; Walter, Hertel, Tannock, Lis, Munro & Hammes 2001; Holben, Williams, Saarinen, Särkilahti & Apajalahti 2002; Temmerman, Huys & Swings 2004; Kim, Brunt & Austin 2007; Peter & Sommaruga 2008). Most of the recent studies have successfully used these techniques alone or in combination with conventional methods to characterize both culturable and unculturable microbiota in the GI tract of fish (Huber, Spanggaard, Appel, Rossen, Nielsen & Gram 2004; Pond, Stone & Alderman 2006; Seppola, Olsen, Sandaker, Kanapathippillai, Holzapfel & Ringo 2006; Shiina, Itoi, Washio & Sugita 2006; Skrodenyte-Arbaciauskiene, Sruoga & Butkauskas 2006; Hovda, Lunestad, Fontanillas & Rosnes 2007; Namba, Mano & Hirose 2007; Liu, Zhou, Yao, Shi, He, Holvold & Ringo 2008; Skrodenyte-Arbaciauskiene, Sruoga, Butkauskas & Skrupskelis 2008; Merrifield, Burnard, Bradley, Davies & Baker 2009), and are presented in Table 1.

Table 1. Different culture-dependent and -independent methods used to study the whole and/or the specific gastrointestinal microorganisms of fish

Sl. No	Fish	Methods of study	References
1	Rainbow trout (Oncorhynchus mykiss)	Culture-based isolation, followed by partial 16S rRNA gene sequencing	Merrifield et al. (2009)
		Culture-independent analysis of 16S rRNA gene sequence by denaturing gradient gel electrophoresis (DGGE)
		Scanning electron microscopic study
2	Atlantic salmon (Salmo salar)	Culture-based isolation and characterization by RFLP analysis of 16S rRNA gene and intergenic spacer region profiles	Navarrete et al. (2009)
2	Atlantic salmon (Salmo salar)	Culture-independent analysis by temporal temperature gradient gel electrophoresis of the 16S rRNA gene and intergenic spacer region profiles	Navarrete et al. (2009)
3	Atlantic Cod (Gadus morhua)	Culture-based isolation and biochemical, physiological characterization and partial sequence analysis of the rpoB and 16S rRNA genes by DGGE	Reid et al. (2009)
4	Grouper (Epinephelus coioides)	Culture-based isolation and biochemical and physiological characterization, followed by 16S rRNA gene analysis	Sun et al. 2009
5	Antarctic notothenioid fish (Notothenia coriiceps, Chaenocephalus aceratus)	Culture-independent analysis of the 16S rRNA gene	Ward et al. (2009)
6	S. salar	Culture-independent analysis of the 16S rRNA gene by DGGE	Liu et al. (2008)
7	Sea trout (Salmo trutta trutta), S. salar	Culture-based isolation and characterization by 16S rRNA gene analysis	Skrodenyte-Arbaciauskiene et al. (2008)
8	S. salar	Culture-based isolation and biochemical and physiological characterization, followed by 16S rRNA gene analysis	Ringø, Sperstad, Kraugerud and Krogdahl (2008)
8	S. salar	Transmission electron microscopic study	Ringø, Sperstad, Kraugerud and Krogdahl (2008)
9	Goldfish (Carassius auratus), Common carp (Cyprinus carpio), Mozambique tilapia (Oreochromis mossambicus), Japanese catfish (Silurus asotus), grass carp (Ctenopharyngodon idella)	Culture-based isolation and characterization by biochemical reactions including API ZYM and API 20A systems as well as by 16S rRNA gene analysis	Tsuchiya et al. (2008)
10	G. morhua	Culture-independent analysis of 16S rRNA gene analysis by DGGE	Brunvold et al. (2007)
11	G. morhua	Culture-based isolation and phenotypic characterization along with 16S rRNA gene analysis	Fjellheim et al. (2007)
12	S. salar	Culture-based isolation and characterization using API 20E and API 20NE systems along with 16S rRNA gene analysis by DGGE	Hovda et al. (2007)
12	S. salar	Culture-independent analysis of 16S rRNA gene by DGGE	Hovda et al. (2007)
13	O. mykiss	Culture-based isolation and characterization by 16S rRNA gene analysis	Kim et al. (2007)
13	O. mykiss	Culture-independent analysis of 16S rRNA gene by DGGE and 16S rDNA clone library techniques	Kim et al. (2007)
14	Senegalese sole (Solea senegalensis)	Culture-based isolation and biochemical characterization using the API 20NE system and also by 16S rRNA gene analysis	Martin-Antonio et al. 2007
15	C. carpio	Culture-based isolation and phenotypical characterization along with 16S rRNA gene analysis	Namba et al. (2007)
16	O. mykiss	Culture-based isolation and characterization using the Biolog system, API strips and 16S rRNA gene analysis	Pond et al. 2006
16	O. mykiss	Culture-independent analysis of 16S rRNA gene by restriction fragment length polymorphism (RFLP)	Pond et al. 2006
17	G. morhua	Culture-based isolation and phenotypic characterization and also by 16S rRNA gene analysis	Ringøet al. 2006a
17	G. morhua	Electron microscopic study	Ringøet al. 2006a
18	Coho Salmon (Oncorhynchus kisutch)	Culture-based isolation and characterization by RFLP analysis of the 16S rRNA gene	Romero and Navarrete (2006)
18	Coho Salmon (Oncorhynchus kisutch)	Culture-independent analysis of the 16S rRNA gene by DGGE	Romero and Navarrete (2006)
19	G. morhua	Culture-based isolation and phenotypic characterization in combination with random amplification of polymorphic – DNA (RAPD) analysis	Seppola et al. (2006)
20	Takifugu niphobles	Culture-based quantitative study, Culture-independent characterization of 16S rRNA gene analysis using the clonal library method	Shiina et al. (2006)
21	River trout (Salmo trutta fario)	Culture-based isolation and characterization by partial 16S rRNA gene sequence analysis	Skrodenyte-Arbaciauskiene et al. (2006)
22	Japanese flounder (Paralichthys olivaceus)	Culture-based isolation and characterization by biochemical and physiological assays, followed by 16S rRNA gene analysis	Sugita and Ito (2006)
23	Bluegill (Lepomis macrochirus)	Culture-independent study by community-level physiological profile analysis using Biolog microplates and analysis of the 16S rRNA gene by TGGE	Uchii et al. (2006)
24	Deepbodied crucian carp (Carassius uvieri), Channel catfish (Ictalurus punctatus), Silver carp (Hypophthalmichthys molitrix), C. carpio	Culture-based isolation and characterization by RAPD analysis of the 16S rRNA gene	Hagi et al. (2004)
25	O. mykiss	Culture-based isolation and characterization by RAPD analysis of the 16S rRNA gene	Huber et al. (2004)
25	O. mykiss	Culture-independent study by fluorescent in situ hybridization (FISH) and DGGE	Huber et al. (2004)
26	C. auratus, C. carpio O. mossambicus	Culture-based isolation and characterization using the whole-cell hybridization technique using rRNA-targeted oligonucleotide probes	Asfie et al. (2003)
26	C. auratus, C. carpio O. mossambicus	Culture-independent analysis of fecal samples by FISH	Asfie et al. (2003)
27	Atlantic halibut (Hippoglossus hippoglossus)	Culture-based isolation and characterization using biochemical and the Biolog GN bacterial identification system as well as RFLP analysis of the 16S rRNA gene and the partial 16S rDNA gene	Verner-Jeffreys et al. (2003)
28	S. salar	Culture-independent study by partial 16S rRNA gene sequence analysis	Holben et al. (2002)
29	Arctic charr (Salvelinus alpines)	Electron microscopic study	Ringøet al. (2001)
30	O. mykiss	Culture-based isolation and characterization using biochemical nature as well as RAPD analysis of the 16S rRNA gene	Spanggaard et al. (2000)

The culture-dependent and -independent studies indicate that bacteria are the major microbial colonizer in the GI tract of fish (MacDonald et al. 1986; Spanggaard et al. 2000; Molinari et al. 2003; Pond et al. 2006). Besides, yeast is also reported to colonize in the GI tract of some fish (Andlid, Vazquez-Juarez & Gustafsson 1998; Gatesoupe 2007). Yeasts belonging to Rhodotorula species are frequently found in the GI tract of both marine and freshwater fish while Metschnikowia zobelii, Trichosporon cutaneum and Candida tropicalisare are the dominant GI yeast species in marine fish (Gatesoupe 2007). The GI microbiota of fish mainly consists of aerobic or facultative anaerobic microorganisms (Clements 1997; Bairagi, Ghosh, Sen & Ray 2002; Saha, Roy, Sen & Ray 2006), facultative as well as obligate anaerobes, especially Cetobacterium somerae (previously classified as Bacteroides type A), Bacteroidaceae and Clostridium species (Cahill 1990; Sugita, Miyajima & Deguchi 1990; Pond et al. 2006; Tsuchiya, Sakata & Sugita 2008). The predominance of anaerobes in the GI tract of fish like gold fish (Carrrasius auratus), Oncorhynchus mykiss and O. niloticus has been recorded (Sakata, Okabayashi & Kakimoto 1980; Sugita et al. 1989; Spanggaard et al. 2000). Earlier, Trust, Bull, Currie and Buckley (1979) reported equal numbers (10⁷ cells g⁻¹ of gut content) of anaerobic bacteria (Bacteroides and Fusabacterium) and aerobic bacteria (Aeromonas and Pseudomonas) in the GI tract of grass carp (Ctenopharyngodon idella).

The total bacterial load in the GI tract of fish is low in comparison with warm-blooded animals and their number often varies with age, nutrition and environment (Ringøet al. 2003; Gomez & Balcazar 2008). In fish, the approximate viable aerobic and anaerobic bacteria usually vary from 10⁴–10⁹ to 6.6 × 10⁴–1.6 × 10⁹ CFU g⁻¹ intestinal content respectively (Skrodenyte-Arbaciauskiene 2007). Earlier culture-dependent studies in faecal samples of fish indicate the aerobic and anaerobic bacterial load to be 10⁸ and 10⁵ bacteria g⁻¹ of faeces respectively (Trust 1975; Trust et al. 1979; Trust & Sparrow 1974; Austin & Al-Zahrani 1988). Recently, Asfie et al. (2003) reported the variation in the total microbial cells in five goldfish specimens to range from 9.6 × 10⁸ to 6.5 × 10¹⁰ cells g⁻¹ of faeces by FISH. Considering the fact that a large population of GI bacteria in fish is unculturable (Romero & Navarrete 2006; Navarrete et al. 2009), the total bacterial load is higher as recorded from the total culturable heterotrophic bacteria. For instance, Shiina et al. (2006), using direct microscopic enumeration of bacteria with 4′,6-diamidino-2-phenylindole, reported the total bacterial count to vary from 1.0 × 10⁴ to 1.4 × 10⁹ CFU g⁻¹ intestinal content in contrast to 4.7 × 10¹⁰–1.9 × 10¹¹ cells g⁻¹ intestinal content in coastal fish like Ditrema temmincki, Girella punctata, Pseudolabrus japonicas, Sebastes pachycephalus, Takifugu niphobles and Thalassoma cupido. Similarly, Sugita, Kurosaki, Okamura, Yamamoto and Tsuchiya (2005) also reported that the total bacterial load of each coastal fish varied from 2.9 × 10⁹ to 3.0 × 10¹⁰ cells g⁻¹ intestinal content through direct counts regardless of the fish species and their feeding habitat, while the viable counts of intestinal bacteria of these species ranged from 1.9 × 10³ to 4.2 × 10⁹ CFU g⁻¹ intestinal content. Recently, Navarrete et al. (2009) also recorded such type of differences in the total bacterial density in different regions of the GI tract such as stomach, pyloric caeca and intestine of S. salar using epifluorescence microscopy as compared with a culture-dependent technique.

The bacterial composition in the GI tract varies from freshwater to marine water fish, with the predominance of Gram-negative bacteria over Gram-positive bacteria in the intestine of several fish species (Sakata, Uno & Kakimoto 1984; Ringø 1993; Hatha, Kuruvilla & Cheriyan 2000). Aeromonads are mostly associated with the GI tract of freshwater fish (Sugita et al. 1983; Sugita, Nakamura, Tanaka & Deguchi 1994; Wang, He, Live, Hu & Chen 1994; Asfie et al. 2003; Skrodenyte-Arbaciauskiene et al. 2008). In freshwater fish, Aeromonas, Pseudomonas and Bacteroides type A are major colonizers in the GI tract, followed by Plesiomonas, Enterobacteriaceae, Micrococcus, Acinetobacter, Clostridium, Bacteroides type B and Fusarium species (Trust et al. 1979; Lesel 1981; Sugita, Sakata, Ishida, Deguihi & Kadota 1981; Sugita et al. 1985). In contrast to freshwater fish, Vibrio, Pseudomonas, Achromobacter, Corynebacterium, Alteromonas, Flavobacterium and Micrococcus species are predominant in the GI tract of most of the marine fish (Cahill 1990; Onarheim et al. 1994; Blanch, Alsina, Simon & Jofre 1997; Verner-Jeffreys et al. 2003). Among other bacterial groups that colonize in the GI tract of both freshwater and marine fish are LAB (Strom 1988; Strom & Ringø 1993; Pilet, Dousset, Barre, Novel, Des mazeaud & Piard 1995; Balcazar, de Blas, Ruiz-Zarzuela, Vendrell, Girones & Muzquiz 2007). However, they are usually not the dominant component of the GI microbiota (Ringøet al. 1995; Jankauskiene 2000a, b), but under certain conditions like a pond culture system, they can dominate, with an abundance as high as 1.1 × 10⁶ cells g⁻¹ fish body weight, and can form a stable component of the GI tract of fish (Syvokien 1989). A recent study on GI bacteria of fish like Notothenia coriiceps and Chaenocephalus aceratus, which differ in their pelagic distribution and feeding strategies, indicated the dominance of Vibrionanceae (γ-proteobacteria) like that in temperate teleost species (Ward et al. 2009).

Application of a recent molecular technology has provided a major breakthrough in the detection and identification of the microbial composition in the GI ecosystem of many animals including fish. Among the recent technologies, DGGE, a ‘genetic fingerprint’ method based on PCR amplification of 16S rDNA, has been successfully used to study the dynamic behaviour of the dominant microbes in different environments (Griffiths, Melville, Cook & Vincent 2001; Long & Azam 2001; Sandaa, Magnesen, Torkildsen & Bergh 2003). PCR- and DGGE-based identification and characterization provides an accurate picture of the complexity of the GI microbiota of fish (Simpson, McCracken, White, Gaskins & Mackie 1999; Griffiths et al. 2001; Huber et al. 2004; Vanhoutte, Huys, De Brandt, Fahey & Swings 2005; Brunvold et al. 2007; Kim et al. 2007). Apart from culturable Vibrio, Pseudomonas, Janthinobacterium and Acinetobacter species, Hovda et al. (2007) successfully characterized predominant but slow-growing culturable bacteria such as Lactobacillus fermentum, Photobacterium phosphoreum, Lactococcus and Bacillus species in the GI tract of Atlantic salmon (S. salar) using PCR- and DGGE-based techniques. Similarly, Pond et al. (2006) succeeded in characterizing the presence of a number of bacterial species like Stenotrophomonas maltophilia, Pseudomonas picketti, Ralstonia eutrophia and β-Proteobacterium in the GI tract of O. mykiss using 16S rRNA technology.

Nowadays, many new uncultuturable bacteria are being identified using molecular biological tools from the GI tract of fish from freshwater to marine type. Several unknown bacteria like Gram-negative Acinetobacter (A. johnsoni), Chryseobacterium, Ochrobactrum, Psychrobacter (P. luti, P. fozii, P. glacincola, P. psychrophilus and P. cibarius) and Sejongia species (S. antarctica) and Gram-positive bacteria like Arthrobacter (A. agilis and A. psychrolactophilus), Brochothrix (B. thermosphacta), Jeotgailbacillus (J. psychrophilus), Microbacterium and Staphylococcus species (S. equorum spp. linens) in S. salar (Ringø, Sperstad, Myklebust, Mayhew et al. 2006); Mycoplasma and Acinetobacter species (A. junii) in S. salar (Holben et al. 2002); α and β subclass of Proteobacteria in C. auratus (Asfie et al. 2003); Clostridium species (C. gasigenes) in O. mykiss (Pond et al. 2006); Tiedjeia arctica in wild river trout Salmo trutta fario (Skrodenyte-Arbaciauskiene et al. 2008), Psychrobacter species; Delftia acidovorans, Burkholderia cepacia and Erwinia carotovora in grouper (Epinephelus coioides) (Sun, Yang, Ling, Chang & Ye 2009); and A. aurescens and Janibacter species in O. mykiss (Merrifield et al. 2009) are now found to be part of the normal microbiota in the GI tract of those fish.

There still remain doubts about the complete microbial composition and load in the GI of majority fish species, and in the near future, culture-independent molecular tools may be able to provide a more detailed picture of the true complexity in the GI tract of different fish species.

Role of GI microbiota in fish: gnotobiotic approaches

Gnotobiotic models (animals cultured under axenic conditions or with a known microbiota) are excellent tools to study the role GI microbes in host (Marques, Ollevier, Verstraete, Sorgeloos & Bossier 2006; Dierckens, Rekecki, Laureau, Sorgeloos, Boon, Van den Broeck & Bossier 2009). Different gnotobiotic model studies reveal the importance of GI microbiota in nutrient metabolism and absorption, xenobiotic metabolism, regulation of energy balance, epithelial renewal, angiogenesis and development and maturation of the mucosal immune system (Falk, Hooper, Midtvedt & Gordon 1998; Cebra 1999). Like other animals, gnotobiotic/germ-free technology is now developed in fish (Dahm & Geisler 2006; Pham, Kanther, Semova & Rawls 2008) and is also used to study evolutionarily conserved microbiota among vertebrates, to monitor the microbial behaviour, interaction and localization of microbes in the gut, as well as their role in nutrition, epithelial development and immunity (Rawls, Mahowald, Ley & Gordon 2006; Rawls, Mahowald, Goodman, Trent & Gordon 2007).

Gnotobiotic studies in fish indicate the involvement of GI microbiota in epithelial differentiation and maturation. Bates, Mittg, Kuhlman, Baden, Cheesman and Guillemin (2006) observed that the differentiation of gut epithelium is arrested by the lack of brushborder intestinal alkaline phosphatase activity and the maintenance of immature patterns of glycan expression in the absence of the microbiota. Alkaline phosphatase activity, which is a marker of epithelial maturation, as well as mucous-secreting goblet cells and hormone-secreting enteroendocrine cells, the secretory cell lineages, are found to increase significantly in the digestive tract of conventional Danio rerio larvae compared with their gnotobiotic counterparts (Bates et al. 2006). Furthermore, microbes are found to up-regulate the expression of 15 genes involved in DNA replication and cell division for epithelial proliferation (Rawls, Samuel & Gordon 2004). Similarly, a marked difference in the enterocytes has also been observed in germ-free and conventional fish. Rawls et al. (2004) observed consistent morphologic enterocytes in gnotobiotic D. rerio, with the large supranuclear vacuoles filled with clear electron-lucent material and that of conventional fish filled with eosinophilic and electron-dense material. In another study, Rekecki, Dierckens, Laureau, Boon, Bossier and Van den Broeck (2009) observed variations with a slightly higher intestinal epithelium in the midgut consisting of a cuboidal to columnar epithelium in conventional larvae compared with cuboidal to squamous epithelium in the midgut of germ-free larvae of Dicentrarchus labrax after the ninth day post hatching.

The GI microbiota plays a crucial role in the nutrition of the host and in fish, they are involved in nutrient metabolism, especially in cholesterol metabolism and trafficking. It has been reported that gnotobiotic D. rerio larvae failed in the uptake of protein macromolecules, with a significant difference in the levels of farnesyldiphosphate synthetase and apolipoprotein B as compared with conventional larvae (Bates et al. 2006). Furthermore, the microbial upregulation of apolipoprotein B, which plays a pivotal role in intra- and extracellular cholesterol trafficking, and downregulation of the liver-specific cholesterol 7α-hydrolase, which catalyses the first step in cholesterol catabolism and bile acid biosynthesis, indicate the microbial modulation of cholesterol metabolism and trafficking (Rawls et al. 2004; Bates et al. 2006).

Besides these, gnotobiotic studies also indicate the involvement of GI microbes in fish immunity and also in xenobitic metabolism. Microbial regulation of glycoprotein production in the GI tract is reported in D. labrax (Rekecki et al. 2009). Furthermore, microbiota are found to up-regulate the genes involved in innate immunity parameters such as serum amyloid A1, C-reactive protein, complement component 3, angiogenin 4, glutathione peroxidase and myeloperoxidase (Rawls et al. 2004; Rawls et al. 2007). Although gnotobiotic studies reveal some of the functional roles of GI microbiota in fish, the full extent to which the microbiota influences gut development, local as well as systemic immunity and homeostasis at the cellular and molecular levels remains to be explored.

Role of GI microbiota in immunity

The gut immune system, which is known as gut-associated lymphoid tissues (GALT), not only provides defence against infectious agents but also regulates immunity in the alimentary tract. The GI microbes play a critical role in the development and maturation of GALT, which in turn mediate a variety of host immune functions (Rhee, Sethupathi, Driks, Lanning & Knight 2004). A complex and integrated interaction between the epithelium, immune components in the mucosa and microbes is responsible for the development and maturation of the gut-associated immune system of the host. Gnotobiotic studies in different animal models also support this notion (Umesaki & Setoyama 2000; Peterson, McNulty, Guruge & Gordon 2007). Several mechanisms are proposed for the involvement of GI bacteria in the development of GALT. Bacteria could stimulate B cell proliferation in GALT through a classical antigen-specific immune response like protein A of Staphylococcus aureus and protein L of Peptostreptococcus magnus (Nilson, Solomon, Bjorck & Akerstrom 1992; Silverman & Goodyear 2002) or by directly stimulating the innate immune system (Medzhitov & Janeway 1997; Leadbetter, Rifkin, Hohlbaum, Beaudette, Shlomchik & Marshak-Rothstein 2002). In fish, GALT consists principally of lymphocytes, eosinophil granular cells, several types of granulocytes and plasma cells (Zapata & Amemiya 2000; Zapata, Diez, Cejalvo, Gutierrez-de & Cortes 2006). The involvement of GI microbes in the epithelial proliferation, maturation and immunity of fish has already been discussed in the gnotobiotic studies (Rawls et al. 2004; Rekecki et al. 2009). Similarly, the endocytosis of bacteria by epithelial cells in the hindgut of immature larvae (Hansen, Strom & Olafsen 1992) as well as intact uptake of bacterial antigens in columnar epithelial cells in the foregut, followed by their penetration into the gut epithelium, have been recorded in fish (Olafsen & Hansen 1992). All these factors may directly or indirectly contribute to the development and stimulation of the immune system.

The early exposure of the intestine to live bacteria and subsequent colonization is very important for the development of gut barrier. In fish, dietary supplementation of useful microbes (probiotics) at early developmental stages can be helpful in increasing the subpopulations of specific acidophilic granulocytes (Picchietti, Mazzini, Taddei, Renna, Fausto, Mulero, Carnevali, Cresci & Abelli 2007). Although probiotics are often found in a transient state and persist for a certain period in the GI tract after the withdrawal of feed in fish, it is worth noting that dietary supplementation of probiotics can enhance both local as well as systemic immunity in a wide range of fish species (Panigrahi, Kiron, Puangkaew, Kobayashi, Satoh & Sugita 2005; Nayak, Swain & Mukherjee 2007; Panigrahi, Kiron, Satoh, Hirono, Kobayashi, Sugita, Puangkaew & Aoki 2007; Picchietti et al. 2007; Aly, Ahmed, Ghareeb & Mohamed 2008; Picchietti, Fausto, Randelli, Carnevali, Taddei, Buonocore, Scapigliati & Abelli 2009; Sharifuzzaman & Austin 2009; Son, Changa, Wu, Guu, Chiu & Cheng 2009).

Role of GI microbiota in nutrition

The importance of intestinal bacteria in the nutrition and well-being of their hosts has been established in several animals (Floch, Gorbach & Lucky 1970). The ability to synthesize vitamins and essential growth factors and digestive enzymes by GI microorganisms has been demonstrated (Teply, Krehi & Elvehjem 1947; Uphill, Jalob & Lall 1977; Drasar & Barrow 1985; Brock, Madigan, Martinko & Parker 1997).

The GI microbiota of hydrobionts has been reported to contribute to the nutrition and physiological processes of the host by producing vitamins, amino acids, digestive enzymes and metabolites, similar to that of mammals (Syvokiene 1989; Cahill 1990; Sugita et al. 1990; Sugita, Matsuo, Hirose, Iwato & Deguchi 1997; Mickeniene 1999; Skrodenyte-Arbaeiauskiene 2000; Skrodenyte-Arbaeiauskiene et al. 2006). Nevertheless, a wide range of enzymes like carbohydrases, phosphatases, esterases, lipases and peptidases, cellulase, lipase and proteases (Bairagi et al. 2002; Ramirez & Dixon 2003; Izvekova & Lapteva 2004) produced by GI bacteria could be a contributory source to digestive enzymes in fish. The presence of a high concentration of Aeromonas in the GI tract can play an important role in digestion as Aeromonas species secrete several proteases (Pemberton, Kidd & Schmidt 1997). Similarly, the p-nitrophenyl-β-n-acetylglucosaminide-, chitin-, cellulose- and collagen-degrading ability of gut bacteria indicates their possible involvement in the nutrition of fish (Shcherbina & Kazlawlene 1971; Lindsay & Harris 1980; Lesel, Fromageot & Lesel 1986; Macdonald et al. 1986; Das & Tripathi 1991; Kar & Ghosh 2008).

Recent studies indicate that anaerobic bacteria might play a role in the digestion and absorption of nutrients (Ramirez & Dixon 2003). Anaerobic bacteria can contribute to fish nutrition by supplying it with volatile fatty acids (Clements 1997). This is due to the fact that volatile fatty acids, end products of anaerobic fermentation, are often reported in the intestines of carp (C. carpio), shad (Dorosoma cepedianum) and largemouth bass (Micropterus salmoides) (Smith, Wahl & Mackie 1996). Nevertheless, the ability of GI aerobic, anaerobic and facultative aerobic bacteria to synthesize different vitamins and amino acids in fish like C. carpio, C. auratus, I. punctatus and O. nilotica is noteworthy (Kashiwada & Teshima 1966; Teshima & Kashiwada 1967; Limsuwan & Lovell 1981; Sugita et al. 1989; Sugita, Miyajima & Deguchi 1991a; Sugita, Takahashi, Miyajima & Deguchi 1991b). Among the vitamins, the production of vitamin B₁₂ by GI bacteria is well documented in fish (Sugita et al. 1991a,b; Sugita, Takahashi, Miyajima & Deguchi 1992). The production of vitamin B₁₂ differs from species to species and is correlated with the abundance of more anaerobes as compared with aerobes in the GI tract. Fish like O. nilotica produce more vitamin B₁₂ as compared with I. punctatus due to the presence of more anaerobic bacteria in the gut of former fish than the latter (Sugita et al. 1990). Similarly, a significant difference in daily vitamin B₁₂ synthesis in O. nilotica (11.2 ng kg⁻¹ body weight) and I. punctatus (1.4 ng kg⁻¹ body weight) has also been recorded by Lovell and Limsuwan (1982).

In contrast to endothermic animals, the exact role of gut microbiota in fish nutrition is difficult to conclude because of the complex and variable ecology of the GI tract of fish. Despite recent conventional and gnotobiotic studies that indicate the possible involvement of GI bacteria in several physiological and nutritional functions in fish, more emphasis and/or thorough research is required in order to establish the nutritional importance of the gut microbiota.

Role of GI microbiota in disease outbreak

The gut of an organism usually harbours a diverse population of non-pathogenic, pathogenic and commensal bacteria, which can contribute significantly to the overall health and disease outbreak in a host. In a healthy animal, some microbiota are established and others are transient in the intestine. There occurs a proper balance between the endogenous microbiota of the intestine and the host's control mechanism. However, if this balance is disturbed, several pathogens present in the transient state can establish lethal infections (Sekirov & Finlay 2009). The GI tract, as well as the skin and gills (Birkbeck & Ringø 2005), serves as a major route for entry of several pathogens to establish lethal infections (Sakai 1979; Chair, Dehasque, Vanpoucke, Nelis, Sorgeloos & Be Leenheer 1994; Grisez, Chair, Sorgeloos & Ollevier 1996; Magarinos, Romalde, Noya, Barja & Toranzo 1996; Olsson, Joborn, Westerdahl, Blomberg, Kjelleberg & Conway 1996; Romalde, Magarinos, Nunez, Barja & Toranzo 1996; Ringø, Jutfelt, Kanapathippillai, Bakken, Sundell, Glette, Mayhew, Myklebust & Olsen 2004). The detailed bacterial translocation process and pathogenesis in the GI tract of fish larvae and fry is a complicated process, which has been discussed in detail by Ringø, Myklebustd, Mayhew and Olsen (2007).

In aquaculture, the advent of intensive aquaculture practices led to the outbreak of diseases in all forms of practices ranging from freshwater to marine and warm water to cold water fish (Nicolas, Robic & Ansquer 1989; Youssef, E1-Timawy & Ahmed 1992; Keskin, Keskin & Rosenrhal 1994; Press & Lillehaug 1995; Karunasagar & Karunasagar 1999). The GI tract is believed to be the major route for the onset of diseases like vibriosis, furunculosis, enteric septicaemia and aeromoniasis in fish. A more recent in vitro study based on the kinetics of the bacterial adhesion to mucus also indicates that the GI tract is the one portal of entry for pathogenic Vibrio alginolyticus into large yellow croaker Pseudosciaena crocea (Chen, Yan, Wang, Zhuang & Wang 2008). Ransom, Lannan, Rohovec and Fryer (1984) reported Vibrio anguillarum and Vibrio ordalii, pathogens in the pyloric caeca and throughout the GI tract of naturally infected Pacific salmon. Furthermore, pathogens after attachment and/or colonization in the tract, can damage the intestinal lining by releasing extracellular enzymes or toxins (Ringøet al. 2004), and within a few hours, establish a lethal infection in fish. Pathogens like Edwardsiella ictaluri and several other entero invasive members of Enterobacteriaceae can infect within 25 h by crossing the mucosal membrane in fish (Baldwin & Newton 1993).

Role of GI microbiota in fish health management

For a very long time, it was believed that the activity of intestinal microbiota in the host is correlated with the longevity of host (Metchnikoff 1901). In endothermic animals, the GI microbiota not only aids the digestive function but also acts as a protective barrier against pathogens (Sissons 1989). These microbes in the gut can protect the host by depriving invading pathogens of nutrients and secreting a range of antimicrobial substances. Fish often harbour a wide range of bacteria in their intestine that have the ability to inhibit pathogens (Schroder, Clausen, Sandberg & Raa 1980; Strom 1988; Onarheim & Raa 1990; Westerdahl, Olsson, Kjelleberg & Conway 1991; Olsson, Westerdahl, Conway & Kjellberg 1992; Smith & Davey 1993; Westerdahl, Olsson, Conway & Kjellberg 1994; Austin, Struckey, Robertson, Effendi & Griffith 1995; Bergh 1995; Sugita, Shibuyu, Shimooka & Deguchi 1996; Joborn, Oisson, Westerdahl, Conway & Kjelleberg 1997; Sugita, Matsuo, Hirose, Iwato & Deguchi 1997; Olsson, Joborn, Westerdahl, Blomberg, Kjelleberg & Conway 1998; Sugita, Ishigaki, Iwai, Suzuki, Okano, Matsuura, Asfie, Aono & Deguchi 1998; Robertson, Dowd, Burrels, Williams & Austin 2000; Sugita, Okano, Suzuki, Iwai, Mizukami, Akiyama & Matsuura 2002).

Sugita, Hirose, Matsuo and Deguchi (1998) found that 2.7% of GI bacteria of freshwater fish inhibited different pathogens, while earlier, Sugita et al. (1996) found 3.2% of GI bacterial isolates in freshwater fish to be effective against Aeromonas. Similarly, Westerdahl et al. (1991) recorded a significantly higher proportion of GI bacteria (28%) of turbot (Scophthalmus maximus) that could inhibit pathogens like Listonella anguillarum. A study in Senegalese sole (Solea senegalensis) indicates an increase in the percentage of antagonistic bacteria in the gut once the larvae start to feed, and after 6 weeks, almost 40% of the GI microbiota was antagonistic against pathogens like L. anguillarum and Photobacterium damselae (Makridis, Martins, Vercauteren, Van Driessche, Decamp & Dinis 2005). Besides, bacteria with a broad-spectrum inhibitory activity, i.e. effective against a wide range of pathogens, are also found in the GI tract of fish. Carnobacterium species, a bacterium often isolated from the GI tract of salmonids, is found to inhibit several pathogens like Aeromonas hydrophila, Aeromonas salmonicida, Flavobacterium branchiophilum, P. damselae, V. anguillarum and Streptococcus milleri (Robertson et al. 2000). Similar types of broad-spectrum antagonistic activity are also exhibited by Weissella hellenica, a Gram-positive GI LAB bacterium isolated from Japanese flounder (Paralichthys olivaceus) (Cai, Benno, Nakase & Oh 1998).

Manipulation of GI microbiota in fish

Nowadays, considerable attention is being focused on the manipulation of intestinal microbial composition and their activities through dietary supplementation to improve the overall health status of the host organism. Health-promoting beneficial microorganisms (probiotics), non-digestible substances that selectively stimulate the growth of one or limited health-promoting bacteria in the intestine of the host (prebiotics) and/or a combination of both (synbiotics) are routinely supplemented in feed for better health management in many animals including fish/shellfish. Their roles in nutrition and growth, immunity, intestinal balance and disease resistance in aquatic animals have been reviewed extensively recently (Kesarcodi-Watson, Kaspar, Lategan & Gibson 2008; Merrifield, Dimitroglou, Foey, Davies, Baker, Bøgwald, Castex & Ringø 2010; Ringø, Olsen, Gifstad, Dalmo, Amlund, Hemre & Bakke 2010).

Probiotics concept

Probiotics are beneficial microbes that help to improve the overall health status of the host organism. The term, probiotic, simply means ‘for life’, originating from the Greek words ‘pro’ and ‘bios’ (Gismondo, Drago & Lombardi 1999). The application of probiotics in aquaculture practices has already gained momentum, and nowadays, numerous microorganisms, both from indigenous and exogenous sources, are used as probiotics (Gatesoupe 1999; Gomez-Gil, Rogue & Turnbull 2000; Ahilan, Shine & Santhanam 2004; Salinas, Cuesta, Esteban & Meseguer 2005; Ghosh, Sinha & Sahu 2007; Buntin, Chanthachum & Hongpattarakere 2008; Kesarcodi-Watson et al. 2008). The commonly used probiotics in fish culture practices belong to Saccharomyces, Clostridium, Bacillus, Enteroccus, Lactobacillus, Shewanella, Leuconostoc, Lactococcus, Carnobacterium, Aeromonas and several other species.

In aquaculture, probiotics are administered by feed and/or as a water additive. However, supplementation of probiotics through feed is a better method for the establishment and successful colonization of the probiont in the GI tract of fish (Gildberg, Mikkelsen, Sandaker & Ringø 1997; Joborn et al. 1997; Robertson et al. 2000). On the other hand, the suspension or the bioencapsulation method is best suitable for fish larvae (Gatesoupe 1991, 1993). Likewise, the co-supplementation of probiotics even at a low concentration with live carriers like rotifers is also found to be effective (Gatesoupe 1993). Gatesoupe (1993) recorded better survival of the larvae of S. maximus by feeding them with Bacillus-enriched rotifers. However, the quantitative and qualitative properties of the bacterial biota in live food have to be adjusted to avoid negative effects in order to accomplish successful colonization in the intestinal tract of fish larvae (Keskin et al. 1994; Munro, Henderson, Barbour & Birkbeck 1999). Nevertheless, certain probiotics, when used as a water additive, can exert several beneficial effects in the host. Increased survival and production of channel catfish (I. punctatus) by Bacillus species (Queiroz & Boyd 1998), improved growth and immunity of O. niloticus by Bacillus subtilis and Rhodopseudomonas palustris (Zhou, Tian, Wang & Li 2009), protection of O. mykiss against V. anguillarum by Pseudomonas fluorescencs (Gram, Melchiorsen, Sanggard, Hubber & Nielsen 1999) and other Pseudomonas species (Spanggaard, Huber, Nielsen, Sick, Pipper, Martinussen, Slierendrecht & Gram 2001) are recorded by direct addition of these bacteria to water.

Probiotics can help increase growth by enhancing the feed conversion efficiency, and confer protection against harmful bacteria by competitive exclusion, production of organic acids (formic acid, acetic acid, lactic acid), hydrogen peroxide and several other compounds such as antibiotics, bacteriocins, siderophores and lysozymes (Austin et al. 1995; Sugita et al. 1996; Gildberg et al. 1997; Gibson 1999; Gram et al. 1999). Besides these, probiotics can also effectively trigger the piscine immune system as already described elsewhere in the text.

Prebiotics concept

Prebiotics are usually non-digestible oligosaccharides used as food ingredients to enhance the composition of certain endogenous health-promoting bacteria in the GI tract of the host (Gibson & Roberfroid 1995; Mussatto & Mancilha 2007). Prebiotics help in generating specific microbiota like Bifidobacter and Lactobacillus species in the host (Houdijk, Bosch, Verstegen & Berenpas 1998; Torrecillas, Makol, Caballero, Montero, Robaina, Real, Sweetman, Tort & Izquierdo 2007; Costalos, Kapiki, Apostolou & Papathoma 2008). Fructo-oligosaccharide, galacto-oligosaccharides, mannan-oligosaccharides (MOS), xylo-oligosaccharides (XOS), inulin, lactulose and lactosucrose are the common prebiotics that are being used in different animals and humans (Teitelbaum & Walker 2002; White, Newman, Cromwell & Lindemann 2002; Tuohy, Rouzaud, Bruck & Gibson 2005).

Prebiotics are found to stimulate the growth of specific intestinal bacteria in fish (Mahious, Gatesoupe, Hervi, Metailler & Ollevier 2006; Dimitroglou, Merrifield, Moate, Davies, Spring, Sweetman & Bradley 2009). Furthermore, dietary supplementation of prebiotics like MOS leads to improved growth and immunity in C. carpio (Staykov, Denev & Spring 2005), O. mykiss (Staykov, Spring, Denev & Sweetman 2007) and D. labrax (Torrecillas et al. 2007), and immunity and disease resistance in hybrid striped bass (Morone chrysops×Morone saxatilis) (Li & Gatlin III 2004, 2005). Nevertheless, enhancement of digestive enzymes like protease and amylase in allogynogenetic crucian carp (C. auratus gibelio) by supplementation of XOS (Xu, Wang, Li & Lin 2009) and increase in the thickness of intestinal tunica muscularis by lactosucrose in red sea bream (Pagrus major) (Kihara, Ohba & Sakata 1995) have also been recorded. However, there are some concerns associated with the use of prebiotics in aquaculture practices. Several pathogens as well as opportunistic bacteria can utilize a wide range of carbohydrates and can eventually pose health hazards by proliferating inside the gut by metabolizing the prebiotics (Gatesoupe 2005). Similarly, another major concern for prebiotics is that high concentrations of prebiotics can be harmful as evidenced from the damaging effect of inulin at a high concentration on the enterocytes of Salvelinus alpinus (Olsen, Myklebust, Kryvi, Mayhew & Ringø 2001).

The success of probiotics and prebiotics has led to the concept of ‘synbiotics’, which refer to nutritional supplements combining probiotics and prebiotics to form a symbiotic relationship. The synbiotic combination of Enterococcus faecalis and MOS was found to exhibit several benefits such as better immune responses and survival against V. anguillarum in fish like O. mykiss (Rodriguez-Estrada, Satoh, Haga, Fushimi & Sweetman 2009). Similarly, positive synergistic effects with higher immune responses and disease resistance by feeding a probiotic Bacillus strain with isomaltooligosaccharides to shrimp were also reported (Li, Tan & Mai 2009). However, the growth enhancement and health improvement of fish/shellfish by promoting the growth of certain microbes in the GI tract through prebiotics and/or synbiotics is a beneficial and rational strategy beyond any doubt but their use in aquaculture is still in its infancy (EL-Dakar, Shalaby & Saoud 2007; Hoffmann 2009).

Conclusion

Over the years, substantial literature has been accumulated, albeit sometimes conflicting, on the nature of the GI bacterial communities in different fish species. Although successful application of molecular techniques has shown considerable complexity of the microbial ecosystem with several new bacteria in the GI tract of fish, unculturable bacteria are still poorly characterized in a wide range of fish species. The conventional and gnotobiotic studies indicate the involvement of GI microbiota of fish in several important biological functions such as physiological, nutritional and immunological processes. However, it is necessary to establish the detailed mechanisms that govern the dynamic microbial community of gut and their effects on each other as well as on the host at the molecular level. Furthermore, molecular- and genomic-based knowledge of the composition and functions of the GI microbiota of fish will certainly help to develop strategies for better health management through the manipulation of microbial ecosystem of gut with suitable probiotics/prebiotics/synbiotics.

Acknowledgment

The author is grateful to Professor T. Nakanishi, Laboratory of Fish Pathology, Department of Veterinary Medicine, Nihon University, Japan, for his novel motivation to write this article.

References

Ahilan B., Shine G. & Santhanam R. (2004) Influence of probiotics on the growth and gut microflora load of juvenile Gold fish (Carassius auratus). Asian Fisheries Science 17, 271–278.
Google Scholar
Al-Harbi A.H. & Uddin M.N. (2004) Seasonal variation in the intestinal bacterial flora of hybrid tilapia (Oreochromis niloticus x Oreochromis aureus) cultured in earthen ponds in Saudi Arabia. Aquaculture 229, 37–44.
10.1016/S0044-8486(03)00388-0
Web of Science® Google Scholar
Allen D.A., Austin B. & Colwell R. (1983) Numerical taxonomy of bacterial isolates associated with a freshwater fishery. Journal of General Microbiology 129, 2043–2062.
Web of Science® Google Scholar
Aly S.M., Ahmed Y.A.G., Ghareeb A.A.A. & Mohamed M.F. (2008) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish and Shellfish Immunology 25, 128–36.
10.1016/j.fsi.2008.03.013
CAS PubMed Web of Science® Google Scholar
Andlid T., Vazquez-Juarez R. & Gustafsson L. (1998) Yeasts isolated from the intestine of rainbow trout adhere to and grow in intestinal mucus. Molecular Marine Biology and Biotechnology 7, 115–126.
CAS PubMed Web of Science® Google Scholar
Asfie M., Yoshijima T. & Sugita H. (2003) Characterization of the goldfish fecal microflora by the fluorescent in situ hybridization method. Fisheries Science 69, 21–26.
10.1046/j.1444-2906.2003.00583.x
CAS Web of Science® Google Scholar
Austin B. & Al-Zahrani A.M.J. (1988) The effect of anti microbial compounds on the gastrointestinal microflora of rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology 33, 1–14.
10.1111/j.1095-8649.1988.tb05444.x
CAS Web of Science® Google Scholar
Austin B., Struckey L.F., Robertson P.A.W., Effendi I. & Griffith D.R.W. (1995) A probiotic strain of Vibrio alginolyticus effective in reducing disease caused by Aeromonas salmonicida, Vibrio anguillarum and Vibrio ordalii. Journal of Fish Diseases 18, 93–96.
10.1111/j.1365-2761.1995.tb01271.x
Web of Science® Google Scholar
Bairagi A., Ghosh K., Sen S.K. & Ray A.K. (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquaculture International 10, 109–121.
10.1023/A:1021355406412
CAS Web of Science® Google Scholar
Bakke-McKellep A.M., Koppang E.O., Gunnes G., Sanden M., Hemre G.I., Landsverk T. & Krogdahl A. (2007) Histological, digestive, metabolic, hormonal and some immune factor responses in Atlantic salmon, Salmo salar L., fed genetically modified soybeans. Journal of Fish Diseases 30, 65–79.
10.1111/j.1365-2761.2007.00782.x
CAS PubMed Web of Science® Google Scholar
Baldwin T.J. & Newton J.C. (1993) Pathogenesis of enteric septicemia of channel catfish, caused by Edwardsiella ictaluri. Bacteriologic and light and electron microscopic findings. Journal of Aquatic Animal Health 5, 189–198.
10.1577/1548-8667(1993)005<0189:POESOC>2.3.CO;2
Google Scholar
Balcazar J.L., De Blas I., Ruiz-Zarzuela I., Vendrell D., Girones O. & Muzquiz J.L. (2007) Sequencing of variable regions of the 16S rRNA gene for identification of lactic acid bacteria isolated from the intestinal microbiota of healthy salmonids. Comparative Immunology, Microbiology and Infectious Diseases 30, 111–118.
10.1016/j.cimid.2006.12.001
PubMed Web of Science® Google Scholar
Bates J.M., Mittge E., Kuhlman J., Baden K.N., Cheesman S.E. & Guillemin K. (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Developmental Biology 297, 374–386.
10.1016/j.ydbio.2006.05.006
CAS PubMed Web of Science® Google Scholar
Bell G.R., Hoskins G.E. & Hodgkiss W. (1971) Aspects of characterisation, identification and ecology of the bacterial flora associated with the surface with surface of stream incubating pacific salmon (Oncorhynchus) egg. Journal of Fishery Research Board Canada 28, 1511–1525.
10.1139/f71-232
Web of Science® Google Scholar
Bergh O. (1995) Bacteria associated with early stages of the Halibut, hippoglassium, l., inhibition of a pathogenic Vibrio sp. Journal of Fish Diseases 18, 31–40.
10.1111/j.1365-2761.1995.tb01263.x
Web of Science® Google Scholar
Bignell D.E. (1984) The arthropod gut as an environment for microorganisms. In: Invertebrate-Microbial Interactions (ed. by J.M. Anderson, A.D.M. Raynon & D.W.A. Walton), pp. 205–227. Cambridge University Press, Cambridge, UK.
Google Scholar
Birkbeck T.H. & Ringø E. (2005) Pathogenesis and the gastrointestinal tract of growing fish. In: Microbial Ecology in Growing Animals (ed. by W. Holzapfel & P. Naughton Biology in Growing Animals Series (ed by S.G.Pierzynowski & R. Zabielski), pp. 208–234. Elsevier, Edinburgh, UK.
10.1016/S1877-1823(09)70043-8
Google Scholar
Blanch A.R., Alsina M., Simon M. & Jofre J. (1997) Determination of bacteria associated with reared turbot (Scophthalmus maximus) larvae. Journal of Applied Microbiology 82, 729–734.
10.1046/j.1365-2672.1997.00190.x
Web of Science® Google Scholar
Brock T.D., Madigan M.T., Martinko J.M. & Parker J. (1997) Biology of Microorganism, 8th edn. Prentice hall, Englewood Chiff, NY, USA.
Google Scholar
Brunvold L., Sandaa R., Mikkelsen H., Welde E., Bleie H. & Bergh Q. (2007) Characterisation of bacterial communities associated with early stages of intensively reared cod (Gadus morhua) using denaturing gradient gel electrophoresis (DGGE). Aquaculture 272, 319–327.
10.1016/j.aquaculture.2007.08.053
CAS Web of Science® Google Scholar
Buntin N., Chanthachum S. & Hongpattarakere T. (2008) Screening of lactic acid bacteria from gastrointestinal tracts of marine fish for their potential use as probiotics. Songklanakarin Journal of Science and Technology 30, 141–148.
Google Scholar
Buras N., Duek L., Niv S., Hepher B. & Sandbank E. (1987) Microbiological aspects of fish grown in treated wastewater. Water Resources 12, 1–10.
Google Scholar
Cahill M.M. (1990) Bacterial flora of fishes: a review. Microbial Ecology 19, 21–41.
10.1007/BF02015051
CAS PubMed Web of Science® Google Scholar
Cai Y., Benno Y., Nakase T. & Oh T.K. (1998) Specific probiotic characterisation of Weissella hellenica DS-12 isolated from flounder intestine. Journal of General and Applied Microbiology 44, 311–316.
10.2323/jgam.44.311
CAS PubMed Web of Science® Google Scholar
Campbell A.C. & Buswell J.A. (1983) The intestinal microflora of farmed dover sole (Solea solea) at different stages of fish development. Journal of Applied Bacteriology 55, 215–223.
10.1111/j.1365-2672.1983.tb01318.x
Web of Science® Google Scholar
Cebra J.J. (1999) Influences of microbiota on intestinal immune system development. American Journal Clinical Nutrition 69, S1046–S1051.
10.1093/ajcn/69.5.1046s
PubMed Web of Science® Google Scholar
Chair M., Dehasque M., Vanpoucke S., Nelis H., Sorgeloos P. & BeLeenheer A.P. (1994) An oral challenge for turbot larvae with Vibrio anguillarum. Aquaculture International 2, 270–272.
10.1007/BF00123437
Google Scholar
Chen Q., Yan Q., Wang K., Zhuang Z. & Wang X. (2008) Portal of entry for pathogenic Vibrio alginolyticus into large yellow croaker Pseudosciaena crocea, and characteristics of bacterial adhesion to mucus. Diseases of Aquatic Organisms 80, 181–188.
10.3354/dao01933
PubMed Web of Science® Google Scholar
Clements K.D. (1997) Fermentation and gastrointestinal microorganisms in fishes. In: Gastrointestinal Microbiology, Vol. 1 (Gastrointestinal ecosystems and fermentations) (ed. by R.I. Mackie & B.A. White), pp. 156–198. Chapman and Hall, New York, NY, USA.
10.1007/978-1-4615-4111-0_6
Google Scholar
Costalos C., Kapiki A., Apostolou M. & Papathoma E. (2008) The effect of a prebiotic supplemented formula on growth and stool microbiology of term infants. Early Human Development 84, 45–49.
10.1016/j.earlhumdev.2007.03.001
CAS PubMed Web of Science® Google Scholar
Dahm R. & Geisler R. (2006) Learning from small fry: the zebra fish as a genetic model organism for aquaculture fish species. Marine Biotechnology 8, 1–17.
10.1007/s10126-006-5139-0
PubMed Web of Science® Google Scholar
Das K.M. & Tripathi S.D. (1991) Studies on the digestive enzymes of grass carp, Ctenopharyngodon idella (V). Aquaculture 92, 21–32.
10.1016/0044-8486(91)90005-R
CAS Web of Science® Google Scholar
Delzenne N.M. & Cani P.D. (2008) Gut microflora is a key player in host energy homeostasis. Medical Science (Paris) 24, 505–510.
10.1051/medsci/2008245505
PubMed Web of Science® Google Scholar
Dierckens K., Rekecki A., Laureau S., Sorgeloos P., Boon N., Van den Broeck W. & Bossier P. (2009) Development of a bacterial challenge test in a gnotobiotic sea bass (Dicentrarchus labrax) culture. Environmental Microbiology 11, 526–533.
10.1111/j.1462-2920.2008.01794.x
CAS PubMed Web of Science® Google Scholar
Dimitroglou A., Merrifield D.L., Moate R., Davies S.J., Spring P., Sweetman J. & Bradley G. (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Animal Science 87, 3226–3234.
10.2527/jas.2008-1428
CAS PubMed Web of Science® Google Scholar
DoBell C. (1932) Anton Von Leewenhoek and Big ‘Little Animals’. Harcourt Brace and Company, New York, NY, USA.
Google Scholar
Drasar B.S. & Barrow P.A. (1985) Intestinal Microbiology. Van Nostrand Reinhold, Workingham, UK. 59–75.
Google Scholar
Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E. & Relman D.A. (2005) Diversity of the human intestinal microbial flora. Science 308, 1635–1638.
10.1126/science.1110591
PubMed Web of Science® Google Scholar
EL-Dakar A.Y., Shalaby S.M. & Saoud I.P. (2007) Assessing the use of a dietary probiotic/prebiotic as an enhancer of spinefoot rabbitfish Siganus rivulatus survival and growth. Aquaculture Nutrition 13, 407–412.
10.1111/j.1365-2095.2007.00491.x
Web of Science® Google Scholar
Falk P.G., Hooper L.V., Midtvedt T. & Gordon J.I. (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiology and Molecular Biology Reviews 62, 1157–1170.
CAS PubMed Web of Science® Google Scholar
Finegold S.M., Suher V.L. & Mathisen G.E. (1983) Normal indigenous intestinal flora. In: Human Intestinal Microflora in Health and Disease (ed. by D.J. Hentgens), pp. 3–31. Academic press, New York, NY, USA.
10.1016/B978-0-12-341280-5.50007-0
Google Scholar
Fjellheim A.J., Playfoot K.J., Skjermo J. & Vadstein O. (2007) Vibrionaceae dominates the microflora antagonistic towards Listonella anguillarum in the intestine of cultured Atlantic cod (Gadus morhua L.) larvae. Aquaculture 269, 98–106.
10.1016/j.aquaculture.2007.04.021
Web of Science® Google Scholar
Floch M.N., Gorbach S.L. & Lucky T.D. (1970) Symposium: the intestinal microflora. American Journal of Clinical Nutrition 23, 1425–1540.
CAS PubMed Web of Science® Google Scholar
Gatesoupe F.J. (1991) The use of probiotics in fish hatcheries: results and prospect. Mariculture Committee Paper F: 33.
Google Scholar
Gatesoupe F.J. (1993) Bacillus sp. spores as food additive for rotifer Branchionus plicatilis: improvement of their bacterial environment and their value for larval turbot, Scophthalmus maximus L. Fish Nutrition in Practice, Les Colloques No. 61 (ed. by S.J. Kaushik & P. Luquet), pp. 561–568. Institute National de la Recherche Agronomique, Paris, France.
Web of Science® Google Scholar
Gatesoupe F.J. (1999) The use of probiotics in aquaculture. Aquaculture 180, 147–165.
10.1016/S0044-8486(99)00187-8
Web of Science® Google Scholar
Gatesoupe F.J. (2005) Probiotics and prebiotics for fish culture, at the parting of the ways. Aqua Feeds: Formulation and Beyond 2, 3–5.
Google Scholar
Gatesoupe F.J. (2007) Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267, 20–30.
10.1016/j.aquaculture.2007.01.005
Web of Science® Google Scholar
Geldreich E.E. & Clarke N.A. (1966) Bacterial pollution indicators in the intestinal tract of freshwater fish. Applied Microbiology 14, 429–437.
10.1128/AEM.14.3.429-437.1966
CAS PubMed Web of Science® Google Scholar
Ghosh S., Sinha A. & Sahu C. (2007) Isolation of putative probionts from the intestines of Indian major carps. The Israeli Journal of Aquaculture – Bamidgeh 59, 127–132.
Web of Science® Google Scholar
Gibson G.R. & Roberfroid M.B. (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125, 1401–1412.
10.1093/jn/125.6.1401
CAS PubMed Web of Science® Google Scholar
Gibson L.F. (1999) Bacteriocin activity and probiotic activity of Aeromonas media. Journal of Applied Microbiology Symposium Supplement 85, 2445–2485.
Google Scholar
Gildberg A., Mikkelsen A., Sandaker E. & Ringø E. (1997) Probiotic effect of lactic acid bacteria in the feed on growth and survival of fry of Atlantic cod (Gadusmorhua). Hydrobiologya 352, 279–285.
10.1023/A:1003052111938
Web of Science® Google Scholar
Gismondo M.R., Drago L. & Lombardi A. (1999) Review of probiotics available to modify gastrointestinal flora. International Journal of Antimicrobial Agents 12, 287–292.
10.1016/S0924-8579(99)00050-3
CAS PubMed Web of Science® Google Scholar
Gomez G.D. & Balcazar J.L. (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology 52, 145–154.
10.1111/j.1574-695X.2007.00343.x
CAS PubMed Web of Science® Google Scholar
Gomez-Gil B., Rogue A. & Turnbull J.F. (2000) The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture 191, 259–270.
10.1016/S0044-8486(00)00431-2
Web of Science® Google Scholar
Gram L., Melchiorsen J., Sanggard B., Hubber I. & Nielsen T. (1999) Inhibition of Vibrio anguillarum by Pseudomonas fluorescens AH₂ a possible probiotic treatment of fish. Applied and Environmental Microbiology 65, 969–973.
CAS PubMed Web of Science® Google Scholar
Griffiths S., Melville K., Cook M. & Vincent S. (2001) Profiling of bacterial species associated with haddock larviculture by PCR amplification of 16S rDNA and denaturing gradient gel electrophoresis. Journal of Aquatic Animal Health 13, 355–363.
10.1577/1548-8667(2001)013<0355:POBSAW>2.0.CO;2
Web of Science® Google Scholar
Grisez L., Chair M., Sorgeloos P. & Ollevier F. (1996) Mode of infection and spread of Vibrio anguillarum in turbot Scophthalmus maximus larvae after oral challenge through live feed. Diseases of Aquatic Organisms 26, 181–187.
10.3354/dao026181
Web of Science® Google Scholar
Hagi T., Tanaka D., Iwamura Y. & Hoshino T. (2004) Diversity and seasonal changes in lactic acid bacteria in the intestinal tract of cultured freshwater fish. Aquaculture 234, 335–346.
10.1016/j.aquaculture.2004.01.018
CAS Web of Science® Google Scholar
Hansen G.H., Strom E. & Olafsen J.A. (1992) Effect of different holding regimens on the intestinal microflora of herring (Clupea harengus) larvae. Applied and Environmental Microbiology 58, 461–470.
CAS PubMed Web of Science® Google Scholar
Hatha A.A.M., Kuruvilla S. & Cheriyan S. (2000) Bacterial flora of the intestines of farm raised freshwater fishes Catla catla, Labeo rohita and Ctenopharyngodon idella. Fishery Technology 37, 59–62.
Google Scholar
Hoffmann K. (2009) Stimulating immunity in fish and crustaceans: some light but more shadows. Aqua Culture Asia Pacific Magazine 5, 22–25.
Google Scholar
Holben W.E., Williams P., Saarinen M., Särkilahti L.K. & Apajalahti J.H.A. (2002) Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microbial Ecology 44, 175–185.
10.1007/s00248-002-1011-6
CAS PubMed Web of Science® Google Scholar
Horsley R.W. (1973) The bacterial flora of the Atlantic salmon (Salmo salar L.) in relation to its environment. Journal of Applied Bacteriology 36, 377–386.
10.1111/j.1365-2672.1973.tb04119.x
CAS PubMed Web of Science® Google Scholar
Horsley R.W. (1977) A review of bacterial flora of teleosts and elasmobranches, including methods for its analysis. Journal of Fish Biology 10, 529–553.
10.1111/j.1095-8649.1977.tb04086.x
Web of Science® Google Scholar
Houdijk J.G.M., Bosch M.W., Verstegen M.W.A. & Berenpas H.J. (1998) Effects of dietary oligosaccharides on the growth performance and faecal characteristics of young growing pigs. Animal Feed Science and Technology 71, 5–48.
10.1016/S0377-8401(97)00138-7
Web of Science® Google Scholar
Hovda M.B., Lunestad B.T., Fontanillas R. & Rosnes J.T. (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272, 581–588.
10.1016/j.aquaculture.2007.08.045
CAS Web of Science® Google Scholar
Huber I., Spanggaard B., Appel K.F., Rossen L., Nielsen T. & Gram L. (2004) Phylogenetic analysis and in situ identification of the intestinal microbial community of rainbow trout (Oncorhynchus mykiss, Walbaum). Journal of Applied Microbiology 96, 117–132.
10.1046/j.1365-2672.2003.02109.x
CAS PubMed Web of Science® Google Scholar
Izvekova G.I. & Lapteva N.A. (2004) Microflora associated with the digestive-transport surfaces of fish and their parasitic cestodes. Russian Journal of Ecology 35, 176–180.
10.1023/B:RUSE.0000025968.97632.30
Web of Science® Google Scholar
Jankauskiene R. (2000a) Defence mechanisms in fish: Lactobacillus genus bacteria of intestinal wall in feeding and hibernating carps. Ekologija (Vilnius) 1, 3–6.
Google Scholar
Jankauskiene R. (2000b) The dependence of the species composition of lactoflora in the intestinal tract of carps upon their Age. Acta Zoological Lituanica 10, 78–83.
10.1080/13921657.2000.10512338
Google Scholar
Joborn A., Oisson J.C., Westerdahl A., Conway P.L. & Kjelleberg S. (1997) Colonisation in the fish intestinal tract and production of inhibitory substances in intestinal mucus and fecal extracts by Carnobacterium sp., stain k1. Journal of Fish Diseases 20, 383–392.
10.1046/j.1365-2761.1997.00316.x
Web of Science® Google Scholar
Kar N. & Ghosh K. (2008) Enzyme producing bacteria in the gastrointestinal tracts of Labeo rohita (Hamilton) and Channa punctatus (Bloch). Turkish Journal of Fisheries and Aquatic Sciences 8, 115–120.
Web of Science® Google Scholar
Karunasagar I. & Karunasagar I. (1999) Diagnosis, treatment and prevention of microbial diseases of fish and shellfish. Current Science 76, 387–399.
CAS Web of Science® Google Scholar
Kashiwada K. & Teshima S. (1966) Studies on the production of B vitamins by intestinal bacteria of fish. I. Nicotinic acid, pantothenic acid and vitamin B₁₂ in carp. Bulletin of the Japanese Society of Scientific Fisheries 32, 961–966.
10.2331/suisan.32.961
CAS Google Scholar
Kesarcodi-Watson A., Kaspar H., Lategan M.J. & Gibson L. (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274, 1–14.
10.1016/j.aquaculture.2007.11.019
Web of Science® Google Scholar
Keskin M., Keskin M. & Rosenrhal H. (1994) Pathways of bacterial contamination during egg incubation and larval rearing turbot, Scophthalmus maximus. Journal of Applied Ichthyology 10, 1–9.
10.1111/j.1439-0426.1994.tb00138.x
Web of Science® Google Scholar
Kihara M., Ohba K. & Sakata T. (1995) Trophic effect of dietary lactosucrose on intestinal tunica muscularis and utilization of this sugar by gut microbes in red seabream, Pagrus major, a marine carnivorous teleost, under artificial rearing. Comparative Biochemistry and Physiology 112, 629–634.
10.1016/0300-9629(95)02037-3
PubMed Web of Science® Google Scholar
Kim D., Brunt J. & Austin B. (2007) Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). Journal of Applied Microbiology 102, 1654–1664.
10.1111/j.1365-2672.2006.03185.x
CAS PubMed Web of Science® Google Scholar
Korsnes K., Nicolaisen O., Skar C.K., Nerland A.H. & Bergh Ø. (2006) Bacteria in the gut of juvenile cod Gadus morhua fed live feed enriched with four different commercial diets. ICES Journal of Marine Science 63, 296–301.
10.1016/j.icesjms.2005.10.012
Web of Science® Google Scholar
Leadbetter E.A., Rifkin I.R., Hohlbaum A.M., Beaudette B.C., Shlomchik M.J. & Marshak-Rothstein A. (2002) Chromatin-IgG complexes activate B cells by dual engagement of Ig M and toll-like receptors. Nature 416, 603–607.
10.1038/416603a
CAS PubMed Web of Science® Google Scholar
Lesel R. (1981) Microflora bacterienne de tractus digest if. In: Nutrition Des Poissions (ed. by M. Fontaine), pp. 89–100. NRS, Paris, France.
Google Scholar
Lesel R. & Peringer P. (1981) Influence of temperature on the bacterial microflora in Salmo gairdneri Richardson. Archives in Hydrobiology 93, 109–120.
Web of Science® Google Scholar
Lesel R. & Sechet J. (1982) Influence d'un stress de manipulation sur le transit dela microflore bacterienne digestive chezla truite are-en-ciel Salmo garidneri Richarson. Acta Ecology Applie 3, 23–33.
Web of Science® Google Scholar
Lesel R., Fromageot C. & Lesel M. (1986) Cellulase digestibility in grass carp, Ctenopharyngodon idella and in gold fish, Carassius auratus. Aquaculture 54, 11–17.
10.1016/0044-8486(86)90249-8
CAS Web of Science® Google Scholar
Li P. & Gatlin D.M. III (2004) Dietary brewers yeast and the prebiotic GroBiotic^™ AE influence growth performance, immune responses and resistance of hybrid striped bass (Morone chrysops X M. saxatilis) to Streptococcus iniae infection. Aquaculture 231, 445–456.
10.1016/j.aquaculture.2003.08.021
Web of Science® Google Scholar
Li P. & Gatlin D.M. III (2005) Evaluation of the prebiotic GroBiotic^®-A and brewers yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops X M. saxatilis) challenged in situ with Mycobacterium marinum. Aquaculture 248, 197–205.
10.1016/j.aquaculture.2005.03.005
CAS Web of Science® Google Scholar
Li J., Tan B. & Mai K. (2009) Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei). Aquaculture 291, 35–40.
10.1016/j.aquaculture.2009.03.005
CAS Web of Science® Google Scholar
Limsuwan T. & Lovell R.T. (1981) Intestinal synthesis and absorption of vit B₁₂ in the channel catfish. Journal of Nutrition 111, 2125–2132.
10.1093/jn/111.12.2125
CAS PubMed Web of Science® Google Scholar
Lindsay G.J.H. & Harris J.E. (1980) Carboxymethyl cellulase activity in the digestive tracts of fish. Journal of Fish Biology 6, 219–233.
10.1111/j.1095-8649.1980.tb03700.x
Web of Science® Google Scholar
Liston J. (1957) The occurrence and distribution of bacterial types on flatfish. Journal of General Microbiology 16, 205–216.
10.1099/00221287-16-1-205
PubMed Web of Science® Google Scholar
Liu Y., Zhou Z., Yao B., Shi P., He S., Holvold L.B. & Ringø E. (2008) Effect of intraperitoneal injection of immunostimulatory substances on allochthonous gut microbiota of Atlantic salmon Salmo salar determined using denaturing gradient gel electrophoresis. Aquaculture Research 39, 635–646.
10.1111/j.1365-2109.2008.01934.x
CAS Web of Science® Google Scholar
Long R.A. & Azam F. (2001) Microscale patchiness of bacterioplankton assemblage richness in seawater. Aquatic Microbial Ecology 26, 103–113.
10.3354/ame026103
Web of Science® Google Scholar
Lovell T. & Limsuwan T. (1982) Intestinal synthesis and dietary non essentiality of vit B₁₂ for Tilapia nilotica. Transaction of American Fisheries Society 11, 485–490.
10.1577/1548-8659(1982)111<485:ISADNO>2.0.CO;2
Web of Science® Google Scholar
MacDonald N.L., Stark J.R. & Austin B. (1986) Bacterial flora associated in gastrointestinal tract of Dover Sole (Solea solea) with special emphasis on the possible role of bacteria in nutrition of the host. FEMS Microbiology Letters 35, 107–111.
10.1111/j.1574-6968.1986.tb01508.x
CAS Web of Science® Google Scholar
MacMillan J.R. & Santucci T. (1990) Seasonal trendy in intestinal bacterial flora of farm raised channel catfish. Journal of Aquatic Animal Health 2, 217–222.
10.1577/1548-8667(1990)002<0217:STIIBF>2.3.CO;2
Google Scholar
Magarinos B., Romalde J.L., Noya M., Barja J.L. & Toranzo A.E. (1996) Adherence and invasive capacities of the fish pathogen Pasteurella piscicida. FEMS Microbiology Letters 138, 29–34.
10.1111/j.1574-6968.1996.tb08130.x
CAS PubMed Web of Science® Google Scholar
Mahious A.S., Gatesoupe F.J., Hervi M., Metailler R. & Ollevier F. (2006) Effect of dietary inulin and oligosaccharides as prebiotics for weaning turbot, Psetta maxima (Linnaeus, C. 1758). Aquaculture International 14, 219–229.
10.1007/s10499-005-9003-4
CAS Web of Science® Google Scholar
Makridis P., Martins S., Vercauteren T., Van Driessche K., Decamp O. & Dinis M.T. (2005) Evaluation of candidate probiotic strains for gilthead sea bream larvae (Sparus aurata) using an in vivo approach. Letter in Applied Microbiology 40, 274–277.
10.1111/j.1472-765X.2005.01676.x
CAS PubMed Web of Science® Google Scholar
Marques A., Ollevier F., Verstraete W., Sorgeloos P. & Bossier P. (2006) Gnotobiotically grown aquatic animals: opportunities to investigate host-microbe interactions. Journal of Applied Microbiology 100, 903–918.
10.1111/j.1365-2672.2006.02961.x
CAS PubMed Web of Science® Google Scholar
Martin-Antonio B., Manchado M., Infante C., Zerolo R., Labella A., Alonso C. & Borrego J.J. (2007) Intestinal microbiota variation in Senegalese sole (Solea senegalensis) under different feeding regimes. Aquaculture Research 38, 1213–1222.
10.1111/j.1365-2109.2007.01790.x
CAS Web of Science® Google Scholar
Medzhitov R. & Janeway C. (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91, 295–298.
10.1016/S0092-8674(00)80412-2
CAS PubMed Web of Science® Google Scholar
Merrifield D.L., Burnard D., Bradley G., Davies S.J. & Baker R.T.M. (2009) Microbial community diversity associated with the intestinal mucosa of farmed rainbow trout (Oncoryhnchus mykiss Walbaum). Aquaculture Research 40, 1064–1072.
10.1111/j.1365-2109.2009.02200.x
Web of Science® Google Scholar
Merrifield D.L., Dimitroglou A., Foey A., Davies S.J., Baker R.T.M., Bøgwald J., Castex M. & Ringø E. (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302, 1–18.
10.1016/j.aquaculture.2010.02.007
Web of Science® Google Scholar
Metchnikoff E. (1901) Surlaflore du corps. Human Member Protocol of Manchester Litereture and Philosophical Society 45, 1–38.
Google Scholar
Mickeniene L. (1999) Bacterial flora in the digestive tract of native and alien species of crayfish in Lithuania. Freshwater Crayfish 12, 279–287.
Google Scholar
Mickeniene L. & Syvokiene J. (2008) The impact of zinc on the bacterial abundance in the intestinal tract of rainbow trout (Oncorhynchus mykiss) larvae. Ekologija 54, 5–9.
10.2478/V10055-008-0002-4
CAS Google Scholar
Molinari L.M., Scoaris D. de O., Pedroso R.B., Bittencourt N. de L.R., Nakamura C.V., Ueda-Nakamura T., Abreu Filho B.A.de. & Dias Filho B.P. (2003) Bacterial microflora in the gastrointestinal tract of Nile tilapia, Oreochromis niloticus, cultured in a semi-intensive system. Acta Scientiarum Biological Sciences Maringa 25, 267–271.
Google Scholar
Moriarty D.J.W. (1990) Interactions of microorganisms and aquatic animals, particularly the nutritional role of the gut flora. In: Microbiology in Poikilotherms (ed. by R. Lesel), pp. 217–222. Elsevier, Amsterdam, the Netherlands.
Google Scholar
Munro P.D., Birkbeck T.H. & Barbour A. (1993) Influence of rate of bacterial colonization of the gut of turbot larvae on larval survival. In: Fish Farming Technology (ed. by H. Reinertsen, L.A. Dahle, L. Jorgensen & K. Tvinnereim), pp. 85–92. A.A. Balkema, Rotterdam, the Netherlands.
Web of Science® Google Scholar
Munro P.D., Barbour A. & Birkbeck T.H. (1994) Comparison of the gut bacterial-flora of start-feeding larval turbot reared under different conditions. Journal of Applied Bacteriology 77, 560–566.
10.1111/j.1365-2672.1994.tb04402.x
Web of Science® Google Scholar
Munro P.D., Henderson R.J., Barbour A. & Birkbeck T.H. (1999) Partial decontamination of rotifers with ultraviolet radiation: the effect of changes in the bacterial load and flora of rotifers on the mortalities in start feeding larval turbot. Aquaculture 170, 229–244.
10.1016/S0044-8486(98)00419-0
Web of Science® Google Scholar
Mussatto S.I. & Mancilha I.M. (2007) Non-digestible oligosaccharides: a review. Carbohydrate Polymers 68, 587–597.
10.1016/j.carbpol.2006.12.011
CAS Web of Science® Google Scholar
Namba A., Mano N. & Hirose H. (2007) Phylogenetic analysis of intestinal bacteria and their adhesive capability in relation to the intestinal mucus of carp. Journal of Applied Microbiology 102, 1307–1317.
10.1111/j.1365-2672.2006.03204.x
CAS PubMed Web of Science® Google Scholar
Navarrete P., Mardones P., Opazo R., Espejo R. & Romero J. (2008) Oxytetracycline treatment reduces bacterial diversity of intestinal microbiota of Atlantic salmon. Journal of Aquatic Animal Health 20, 177–183.
10.1577/H07-043.1
PubMed Web of Science® Google Scholar
Navarrete P., Espejo R.T. & Romero J. (2009) Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microbial Ecology 57, 550–561.
10.1007/s00248-008-9448-x
CAS PubMed Web of Science® Google Scholar
Nayak S.K., Swain P. & Mukherjee S.C. (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham.). Fish and Shellfish Immunology 23, 892–896.
10.1016/j.fsi.2007.02.008
CAS PubMed Web of Science® Google Scholar
Nicholson J.K., Holmes E. & Wilson I.D. (2005) Gut microorganisms, mammalian metabolism and personalized health care. Nature Review on Microbiology 3, 431–438.
10.1038/nrmicro1152
CAS PubMed Web of Science® Google Scholar
Nicolas J.L., Robic E. & Ansquer D. (1989) Bacterial flora associated with a tropic chain consisting of microalgae, rotifers and turbot larval: influence of bacteria on larval survival. Aquaculture 83, 237–248.
10.1016/0044-8486(89)90036-7
Web of Science® Google Scholar
Nieto T.P., Toranzo A.E. & Barja J.C. (1984) Comparison between the bacterial flora associated with fingerling trout, cultured in two different hatcheries in the northwest of spain. Aquaculture 42, 193–206.
10.1016/0044-8486(84)90100-5
Web of Science® Google Scholar
Nilson B.H., Solomon A., Bjorck L. & Akerstrom B. (1992) Protein L from Peptostreptococcus magnus binds to the light chain variable domain. Journal of Biological Chemistry 267, 2234–2239.
CAS PubMed Web of Science® Google Scholar
Ogbondeminu F.S. (1993) The occurrence and distribution of enteric bacteria in fish and water of tropical aquaculture ponds in Nigeria. Journal of Aquaculture in Tropics 8, 61–66.
Google Scholar
Ogbondeminu F.S. & Olayemi A.B. (1993) Antibiotic resistance in enteric bacterial isolates from fish and water media. Journal of Aquaculture in Tropics 8, 207–212.
Google Scholar
Olafsen J.A. & Hansen G.H. (1992) Intact antigen uptake in intestinal epithelial cells of marine fish larvae. Journal of Fish Biology 40, 141–156.
10.1111/j.1095-8649.1992.tb02562.x
Web of Science® Google Scholar
Olsen R.E., Myklebust R., Kryvi H., Mayhew T.M. & Ringø E. (2001) Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.). Aquaculture Research 32, 931–934.
10.1046/j.1365-2109.2001.00626.x
Web of Science® Google Scholar
Olsson J.C., Westerdahl A., Conway P.L. & Kjellberg S. (1992) Intestinal colonization potential of turbot (Scophthalmus maximus) and dab (Limanda limanda) associated bacteria with inhibitory effect against Vibrio anguillarum. Applied and Environmental Microbiology 58, 551–556.
PubMed Web of Science® Google Scholar
Olsson J.C., Joborn A., Westerdahl A., Blomberg L., Kjelleberg S. & Conway P. (1996) Is the turbot intestine, Scophthalmus maximum, L., intestinal a portal of entry for the fish pathogen Vibrio anguillarum. Journal of Fish Diseases 19, 225–234.
10.1111/j.1365-2761.1996.tb00129.x
Web of Science® Google Scholar
Olsson J.C., Joborn A., Westerdahl A., Blomberg L., Kjelleberg S. & Conway P.L. (1998) Survival, persistence and proliferation of Vibrio anguillarum in juvenile turbot Scophthalmus maximus (L.) intestine and faeces. Journal of Fish Diseases 21, 1–9.
10.1046/j.1365-2761.1998.00327.x
CAS PubMed Web of Science® Google Scholar
Onarheim A.M. & Raa J. (1990) Characterization and possible biological significance of autochthonous flora in the intestinal mucosa of seawater fish. In: Microbiology in Poikilotherms (ed. by R. Lesel), pp. 197–201. Elsevier, Amsterdam, The Netherlands.
Google Scholar
Onarheim A.M., Wiik R., Burghardt J. & Stackebradt E. (1994) Characterisation and identification of two Vibrio species indigenous to intestine of fish in cold water, description of Vibrio iliopiscarius sp. nov. syst. Applied Microbiology 17, 370–379.
10.1016/S0723-2020(11)80053-6
Web of Science® Google Scholar
Panigrahi A., Kiron V., Puangkaew J., Kobayashi T., Satoh S. & Sugita H. (2005) The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout Oncorhynchus mykiss. Aquaculture 243, 241–254.
10.1016/j.aquaculture.2004.09.032
Web of Science® Google Scholar
Panigrahi A., Kiron V., Satoh S., Hirono I., Kobayashi T., Sugita H., Puangkaew J. & Aoki T. (2007) Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Developmental and Comparative Immunology 31, 372–382.
10.1016/j.dci.2006.07.004
CAS PubMed Web of Science® Google Scholar
Pemberton J.M., Kidd S.P. & Schmidt R. (1997) Secreted enzymes of Aeromonas. FEMS Microbiology Letters 152, 1–10.
10.1111/j.1574-6968.1997.tb10401.x
CAS PubMed Web of Science® Google Scholar
Peter H. & Sommaruga R. (2008) An evaluation of methods to study the gut bacterial community composition of freshwater zooplankton. Journal of Plankton Research 30, 997–1006.
10.1093/plankt/fbn061
Web of Science® Google Scholar
Peterson D.A., McNulty N.P., Guruge J.L. & Gordon J.I. (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host and Microbe 2, 328–339.
10.1016/j.chom.2007.09.013
CAS PubMed Web of Science® Google Scholar
Pham L.N., Kanther M., Semova I. & Rawls J.F. (2008) Methods for generating and colonizing gnotobiotic zebrafish. Nature Protocols 3, 1862–1875.
10.1038/nprot.2008.186
CAS PubMed Web of Science® Google Scholar
Picchietti S., Mazzini M., Taddei A.R., Renna R., Fausto A.M., Mulero V., Carnevali O., Cresci A. & Abelli L. (2007) Effects of administration of probitoc strains on GALT of larval gilthead seabream: immnohistochemical and ultrastructural studies. Fish and Shellfish Immunology 22, 57–67.
10.1016/j.fsi.2006.03.009
CAS PubMed Web of Science® Google Scholar
Picchietti S., Fausto A.M., Randelli E., Carnevali O., Taddei A.R., Buonocore F., Scapigliati G. & Abelli L. (2009) Early treatment with Lactobacillus delbrueckii strain induces an increase in intestinal T-cells and granulocytes and modulates immune-related genes of larval Dicentrarchus labrax (L.). Fish and Shellfish Immunology 26, 368–376.
10.1016/j.fsi.2008.10.008
CAS PubMed Web of Science® Google Scholar
Pilet M.F., Dousset X., Barre R., Novel G., Des mazeaud M. & Piard J.C. (1995) Evidence for two bacteriocins produced by Carnobacterium piscicola and Carnobacterium divergens isolated from fish and active against Listeria monocytogenes. Journal of Food Protection 58, 256–262.
10.4315/0362-028X-58.3.256
Web of Science® Google Scholar
Pond M.J., Stone D.M. & Alderman D.J. (2006) Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Aquaculture 261, 194–203.
10.1016/j.aquaculture.2006.06.037
CAS Web of Science® Google Scholar
Press C.M. & Lillehaug A. (1995) Vaccination in European salmonid aquaculture: a review of practices and prospects. British Veterinary Journal 151, 45–69.
10.1016/S0007-1935(05)80064-8
PubMed Web of Science® Google Scholar
Queiroz J.F. & Boyd C.E. (1998) Effects of a bacterial inoculum in channel catfish ponds. Journal of World Aquaculture Society 29, 67–73.
10.1111/j.1749-7345.1998.tb00300.x
Web of Science® Google Scholar
Ramirez R.F. & Dixon B.A. (2003) Enzyme production by obligate intestinal anaerobic bacteria isolated from oscars (Astronotus ocellatus), angelfish (Pterophyllum scalare) and southern flounder (Paralichthys lethostigma). Aquaculture 227, 417–426.
10.1016/S0044-8486(03)00520-9
CAS Web of Science® Google Scholar
Ransom D.P., Lannan C.N., Rohovec J.S. & Fryer J.L. (1984) Comparison of histopathology caused by Vibrio anguillarum and Vibrio ordalii in three species of pacific salmon. Journal of Fish Diseases 7, 107–115.
10.1111/j.1365-2761.1984.tb00913.x
Web of Science® Google Scholar
Rastall R.A. (2004) Bacteria in the gut: friends and foes and how to alter the balance. Journal of Nutrition 134, S2022–S2026.
10.1093/jn/134.8.2022S
CAS PubMed Web of Science® Google Scholar
Rawls J.F., Samuel B.S. & Gordon J.I. (2004) Gnotobiotic zebra fish reveal evolutionarily conserved responses to the gut microbiota. Proceedings of the National Academy of Sciences, USA 101, 4596–4601.
10.1073/pnas.0400706101
CAS PubMed Web of Science® Google Scholar
Rawls J.F., Mahowald M.A., Ley R.E. & Gordon J.I. (2006) Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423–433.
10.1016/j.cell.2006.08.043
CAS PubMed Web of Science® Google Scholar
Rawls J.F., Mahowald M.A., Goodman A.L., Trent C.M. & Gordon J.I. (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebra fish gut. Proceedings of the National Academy of Sciences, USA 104, 7622–7627.
10.1073/pnas.0702386104
CAS PubMed Web of Science® Google Scholar
Reid H.I., Treasurer J.W., Adam B. & Birkbeck T.H. (2009) Analysis of bacterial populations in the gut of developing cod larvae and identification of Vibrio logei, Vibrio anguillarum and Vibrio splendidus as pathogens of cod larvae. Aquaculture 288, 36–43.
10.1016/j.aquaculture.2008.11.022
Web of Science® Google Scholar
Reitan K.I., Natvik C.M. & Vadstein O. (1998) Drinking rate, uptake of bacteria and microalgae in turbot larvae. Journal of Fish Biology 53, 1145–1154.
10.1111/j.1095-8649.1998.tb00238.x
Web of Science® Google Scholar
Rekecki A., Dierckens K., Laureau S., Boon N., Bossier P. & Van den Broeck W. (2009) Effect of germ-free rearing environment on gut development of larval sea bass (Dicentrarchus labrax L.). Aquaculture 293, 8–15.
10.1016/j.aquaculture.2009.04.001
Web of Science® Google Scholar
Rhee K.J., Sethupathi P., Driks A., Lanning D.K. & Knight K.L. (2004) Role of commensal bacteria in development of gut associated lymphoid tissues and preimmune antibody repertoire. The Journal of Immunology 172, 1118–1124.
10.4049/jimmunol.172.2.1118
CAS PubMed Web of Science® Google Scholar
Ringø E. (1993) The effect of chromic oxide (Cr₂O₃) on aerobic bacterial population associated with the intestinal epithelial mucosa of arctic charr, Salvilinus alpinus (L). Canadian Journal of Microbiology 39, 1169–1173.
10.1139/m93-177
Web of Science® Google Scholar
Ringø E. & Birkbeck T.H. (1999) Intestinal microflora of fish larvae and fry. Aquaculture Research 30, 73–93.
10.1046/j.1365-2109.1999.00302.x
Web of Science® Google Scholar
Ringø E. & Gatesoupe F.J. (1998) Lactic acid bacteria in fish. A review. Aquaculture 160, 177–203.
10.1016/S0044-8486(97)00299-8
Web of Science® Google Scholar
Ringø E. & Olsen R.E. (1999) The effect of diet on aerobic bacterial flora associated with intestine of arctic charr (Salvelinus alpinus L.). Journal of Applied Microbiology 86, 22–28.
10.1046/j.1365-2672.1999.00631.x
CAS PubMed Web of Science® Google Scholar
Ringø E. & Strom E. (1994) Microflora of arctic charr, Salvilinus alpinus (L). Gastrointestinal microflora of free living fish and effect of diet and salinity on intestinal microflora. Aquaculture and Fish Management 25, 623–629.
10.1111/j.1365-2109.1994.tb00726.x
Google Scholar
Ringø E., Strom E. & Tabachek J.A. (1995) Intestinal microflora of Salmonids. A review. Aquaculture Research 26, 773–789.
10.1111/j.1365-2109.1995.tb00870.x
Google Scholar
Ringø E., Lodemel J.B., Myklebust R., Kaino T., Mayhew T.M. & Olsen R.E. (2001) Epithelium-associated bacteria in the gastrointestinal tract of Arctic charr (Salvelinus alpines L.) - An electron microscopical study. Journal of Applied Microbiology 90, 294–300.
10.1046/j.1365-2672.2001.01246.x
CAS PubMed Web of Science® Google Scholar
Ringø E., Olsen R.E., Mayhew T.M. & Myklebust R. (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227, 395–415.
10.1016/j.aquaculture.2003.05.001
Web of Science® Google Scholar
Ringø E., Jutfelt F., Kanapathippillai P., Bakken Y., Sundell K., Glette J., Mayhew T.M., Myklebust R. & Olsen R.E. (2004) Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L.). Cell and Tissue Research 318, 305–311.
10.1007/s00441-004-0934-2
PubMed Web of Science® Google Scholar
Ringø E., Sperstad S., Myklebust R., Refstie S. & Krogdahl A. (2006) Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261, 829–841.
10.1016/j.aquaculture.2006.06.030
CAS Web of Science® Google Scholar
Ringø E., Sperstad S., Myklebust R., Mayhew T.M. & Olsen R.E. (2006) The effect of dietary inulin on aerobic bacteria associated with hindgut of arctic charr (Salvelinus alpinus L.). Aquaculture Research 37, 891–897.
10.1111/j.1365-2109.2006.01509.x
CAS Web of Science® Google Scholar
Ringø E., Myklebustd R., Mayhew T.M. & Olsen R.E. (2007) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268, 251–264.
10.1016/j.aquaculture.2007.04.047
Web of Science® Google Scholar
Ringø E., Sperstad S., Kraugerud O.F. & Krogdahl A. (2008) Use of 16S rRNA gene sequencing analysis to characterize culturable intestinal bacteria in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy. Aquaculture Research 39, 1087–1100.
10.1111/j.1365-2109.2008.01972.x
CAS Web of Science® Google Scholar
Ringø E., Olsen R.E., Gifstad T.Ø., Dalmo R.A., Amlund H., Hemre G.I. & Bakke A.M. (2010) Prebiotics in aquaculture: a review. Aquaculture Nutrition 16, 117–136.
10.1111/j.1365-2095.2009.00731.x
CAS Web of Science® Google Scholar
Robertson P.A.W., Dowd C.O., Burrels C., Williams P. & Austin B. (2000) Use of Carnobactrium sp. as a probiotic for Atlantic Salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture 18, 235–243.
10.1016/S0044-8486(99)00349-X
Web of Science® Google Scholar
Rodriguez-Estrada U., Satoh S., Haga Y., Fushimi H. & Sweetman J. (2009) Effects of single and combined supplementation of Enterococcus faecalis, mannan oligosaccharide and polyhydrobutyric acid on growth performance and immune response of rainbow trout Oncorhynchus mykiss. Aquaculture Science 57, 609–617.
CAS Google Scholar
Romalde J.L., Magarinos B., Nunez S., Barja J.L. & Toranzo A.E. (1996) Host range susceptibility of enterococcus sp. strains isolated from diseased turbot: possible routes of infection. Applied and Environmental Microbiology 62, 607–611.
CAS PubMed Web of Science® Google Scholar
Romero J. & Navarrete P. (2006) 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of coho salmon (Oncorhynchus kisutch). Microbial Ecology 51, 422–430.
10.1007/s00248-006-9037-9
CAS PubMed Web of Science® Google Scholar
Saha S., Roy R.N., Sen S.K. & Ray A.K. (2006) Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (P) and grass carp, Ctenopharyngodon idella (V). Aquaculture Research 37, 380–388.
10.1111/j.1365-2109.2006.01442.x
CAS Web of Science® Google Scholar
Sakai D.K. (1979) Invasive routes of Aeromonas salmonicida salmonid furuculorts: exl sub sp. salmonicida. Scientific Reports of the Hokkaido fish Hatchery 34, 1–6.
Google Scholar
Sakata T. (1989) Microflora of healthy animals. In: Methods for Microbilogical Examinations (ed. by B. Austin & D.A. Austin), pp. 141–163. John Wiley and Sons, New York, NY, USA.
Google Scholar
Sakata T. (1990) Microflora in the digestive tract of fish and shell fish. In: Microbiology in Poikiloterms (ed. by R. Lessel), pp. 171–176. Elsevier, Amsterdam, The Netherlands.
Google Scholar
Sakata T., Okabayashi J. & Kakimoto D. (1980) Variations in the intestinal microflora of tilapia reared in fresh and sea water. Bulletin of the Japanese Society of Scientific Fisheries 46, 313–317.
10.2331/suisan.46.313
Web of Science® Google Scholar
Sakata T., Sugita H., Mitsuoka T., Kakimoto D. & Kadota H. (1981) Characteristics of obligate anaerobic bacteria in the intestines of freshwater fish. Bulletin of the Japanese Society of Scientific Fisheries 47, 421–427.
10.2331/suisan.47.421
CAS Web of Science® Google Scholar
Sakata T., Uno K. & Kakimoto D. (1984) Dominant bacteria of the aerobic microflora in tilapia intestine. Bulletin of Japanese Society of Scientific Fisheries 50, 489–493.
10.2331/suisan.50.489
Web of Science® Google Scholar
Salinas I., Cuesta A., Esteban M.A. & Meseguer J. (2005) Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish and Shellfish Immunology 19, 67–77.
10.1016/j.fsi.2004.11.007
CAS PubMed Web of Science® Google Scholar
Sandaa R.A., Magnesen T., Torkildsen L. & Bergh O. (2003) Characterisation of bacterial communities associated with early life stages of cultured great scallop (Pecten maximus), using denaturing gradient gel electrophoresis (DGGE). Systematic and Applied Microbiology 26, 302–311.
10.1078/072320203322346164
PubMed Web of Science® Google Scholar
Savage D.C. (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology 31, 107–133.
10.1146/annurev.mi.31.100177.000543
CAS PubMed Web of Science® Google Scholar
Savage D.C. (1989) The normal human microflora composition. In: The Regulatory and Protective Role of the Normal Microflora (ed. by R. Grubb, T. Midvedt & E. Norin), pp. 3–18. Stockton press, New York, NY, USA.
10.1007/978-1-349-10723-0_1
Web of Science® Google Scholar
Schroder K., Clausen E., Sandberg A.M. & Raa J. (1980) Psychotropic Lactrobacillus plantarum from fish and its ability to produce antibiotic substances. In: Advances in Fish Science and Technology (ed. by J.J. Connell), pp. 480–483. Fishery News Books Ltd., Farnham, Surrey, UK.
Web of Science® Google Scholar
Sekirov I. & Finlay B.B. (2009) The role of the intestinal microbiota in enteric infection. Journal of Physiology 587, 4159–4167.
10.1113/jphysiol.2009.172742
CAS PubMed Web of Science® Google Scholar
Seppola M., Olsen R.E., Sandaker E., Kanapathippillai P., Holzapfel W. & Ringø E. (2006) Random amplification of polymorphic DNA (RAPD) typing of Carnobacteria isolated from hindgut chamber and large intestine of Atlantic cod (Gadus morhua L.). Systematic and Applied Microbiology 29, 131–137.
10.1016/j.syapm.2005.07.006
CAS PubMed Web of Science® Google Scholar
Sera H., Ishida Y. & Kadota H. (1974) Bacterial flora in the digestive tracts of marine fish. In: Effect of the Ocean Environment on Microbial Activities (ed. by R.R. Colwell & R.Y. Morita), pp. 467–490. University Park Press, Baltimore, MD, USA.
Google Scholar
Sharifuzzaman S.M. & Austin B. (2009) Influence of probiotic feeding duration on disease resistance and immune parameters in rainbow trout. Fish and Shellfish Immunology 27, 440–445.
10.1016/j.fsi.2009.06.010
CAS PubMed Web of Science® Google Scholar
Shcherbina M.A. & Kazlawlene O.P. (1971) The reaction of the medium and the rate of absorption of nutrients in the intestine of carp. Journal of Ichthyology 11, 81–85.
Google Scholar
Shiina A., Itoi S., Washio S. & Sugita H. (2006) Molecular identification of intestinal microflora in Takifugu niphobles. Comparative Biochemistry and Physiology (Part D) 1, 128–132.
PubMed Web of Science® Google Scholar
Silverman G.J. & Goodyear C.S. (2002) A model B-cell superantigen and the immunobiology of B lymphocytes. Clinical Immunology 102, 117–134.
10.1006/clim.2001.5143
CAS PubMed Web of Science® Google Scholar
Simpson J.M., McCracken V.J., White B.A., Gaskins H.R. & Mackie R.I. (1999) Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. Journal Microbiological Methods 36, 167–179.
10.1016/S0167-7012(99)00029-9
CAS PubMed Web of Science® Google Scholar
Sissons J.W. (1989) Potential of probiotic organisms to prevent diarrhoea and promote digestion in farm animals – A review. Journal of Science and Food in Agriculture 49, 1–13.
10.1002/jsfa.2740490102
Web of Science® Google Scholar
Sivakami R., Premkishore G. & Chandran M.R. (1996) Occurrence and distribution of potentially pathogenic Enterobacteriaceae in carps and pond water in Tamil Nadu, India. Aquaculture Research 27, 375–378.
10.1111/j.1365-2109.1996.tb01263.x
Google Scholar
Skrodenyte-Arbaeiauskiene V. (2000) Proteolytic activity of the roach (Rutilus rutilus L.) intestinal microflora. Acta Zoologica Lituanica 10 (3), 69–77.
10.1080/13921657.2000.10512337
Google Scholar
Skrodenyte-Arbaciauskiene V. (2007) Enzymatic activity of intestinal bacteria in roach Rutilus rutilus L. Fisheries Science 73, 964–966.
10.1111/j.1444-2906.2007.01421.x
CAS Web of Science® Google Scholar
Skrodenyte-Arbaciauskiene V., Sruoga A & Butkauskas D. (2006) Assessment of microbial diversity in the river trout Salmo trutta fario L. intestinal tract identified by partial 16S rRNA gene sequence analysis. Fisheries Science 72, 597–602.
10.1111/j.1444-2906.2006.01189.x
CAS Web of Science® Google Scholar
Skrodenyte-Arbaciauskiene V., Sruoga A., Butkauskas D. & Skrupskelis K. (2008) Phylogenetic analysis of intestinal bacteria of freshwater salmon Salmo salar and sea trout Salmo trutta and diet. Fisheries Science 74, 1307–1314.
10.1111/j.1444-2906.2008.01656.x
CAS Web of Science® Google Scholar
Smith H. & Davey S. (1993) Evidence for competitive exclusion of Aeromonas salmonicida from fish with stress inducible furunculosis by a florescent pseudomonas. Journal of Fish Diseases 16, 521–524.
10.1111/j.1365-2761.1993.tb00888.x
Web of Science® Google Scholar
Smith T.B., Wahl D.H. & Mackie R.I. (1996) Volatile fatty acids and anaerobic fermentation in temperature piscivorous and omnivorous freshwater fish. Journal of Fish Biology 48, 829–841.
10.1111/j.1095-8649.1996.tb01479.x
CAS Web of Science® Google Scholar
Son V.M., Changa C.C., Wu M.C., Guu Y.K., Chiu C.H. & Cheng W. (2009) Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish and Shellfish Immunology 26, 691–698.
10.1016/j.fsi.2009.02.018
CAS PubMed Web of Science® Google Scholar
Spanggaard B., Huber I., Nielsen J., Nielsen L., Applel K. & Gram L. (2000) The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 182, 1–15.
10.1016/S0044-8486(99)00250-1
CAS Web of Science® Google Scholar
Spanggaard B., Huber I., Nielsen J., Sick E.B., Pipper C.B., Martinussen T., Slierendrecht W. & Gram L. (2001) The probiotic potential against vibriosis of the indigenous microflora of rainbow trout. Environmental Microbiology 3, 755–765.
10.1046/j.1462-2920.2001.00240.x
CAS PubMed Web of Science® Google Scholar
Staykov Y., Denev S. & Spring P. (2005) Influence of dietary mannan oligosaccharides (Bio-Mos) on growth rate and immune function of common carp (Cyprinus carpio L.). In : Lessons From the Past to Optimise the Future (Special Publication No 35, June 2005) (ed. by B. Howell & R. Flos), pp. 431–432. European Aquaculture Society, Belgium.
Google Scholar
Staykov Y., Spring P., Denev S. & Sweetman J. (2007) Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquaculture International 15, 153–161.
10.1007/s10499-007-9096-z
CAS Web of Science® Google Scholar
Strom E. (1988) Melkesyrebakt'erier I fb ketarm. Isolasjon, Karaktesisies og egnekaper. Thesis, the Norwegian College of Fishery Science, Tromso.
Google Scholar
Strom E. & Ringø E. (1993) Changes in the bacterial composition of early developing cod, Gadus mohua (L.) larvae following inoculation of Lactobaccilus plantarum into the water. In: Physiological and Biochemical Aspects of Fish Development (ed. by B. Walther & H.J. Fyn), pp. 226–228. Grasfisk Hus, Bergen, Norway.
Google Scholar
Sugita H. & Ito Y. (2006) Identification of intestinal bacteria from Japanese flounder (Paralichthys olivaceus) and their ability to digest chitin. Letters in Applied Microbiology 43, 336–342.
10.1111/j.1472-765X.2006.01943.x
CAS PubMed Web of Science® Google Scholar
Sugita H., Sakata T., Ishida Y., Deguihi Y. & Kadota H. (1981) Aerobic and anaerobic bacteria in the intestine of ayu, Pleloglossus altivelis. Bulletin of College of Agriculture and Veterinary Medicine 38, 302–306.
Google Scholar
Sugita H., Enomoto A. & Deguchi Y. (1982) Intestinal microflora in the fry of Tilapia mossambica. Bulletin of the Japanese Society of Scientific Fisheries 48, 875.
10.2331/suisan.48.875
Web of Science® Google Scholar
Sugita H., Isida Y., Deguchi Y. & Kadota H. (1982) Bacterial flora in the gastrointestine of Tilapia nilotica adapted in sea water. Bulletin of the Japanese Society of Scientific Fisheries 48, 987–991.
10.2331/suisan.48.987
Google Scholar
Sugita H., Oshima K., Tamura M. & Deguchi Y. (1983) Bacterial flora in the gastrointestine of freshwater fishes in the river. Bulletin of the Japanese Society of Scientific Fisheries 49, 987–991.
10.2331/suisan.49.1387
Google Scholar
Sugita H., Tokuyama K. & Deguchi Y. (1985) The intestinal microflora of carp Cyprinus carpio, grass carp Ctenopharyngodon idella and tilapia Sarotherodon niloticus. Bulletin of Japanese Society Sciences of Fisheries 50, 1325–1329.
10.2331/suisan.51.1325
Google Scholar
Sugita H., Tsunohara M., Fukumoto M. & Deguchi Y. (1987) Comparison of microflora between intestinal contents and fecal pellets of fresh water fishes. Nippon Suisan Gakkaishi 53, 287–290.
10.2331/suisan.53.287
Web of Science® Google Scholar
Sugita H., Fukumoto M., Koyama H. & Deguchi Y. (1988) Changes in the fecal microflora of gold fish Carassius auratus with the oral administration of oxytetracycline. Bulletin of the Japanese Society of Scientific Fisheries 54, 2181–2187.
10.2331/suisan.54.2181
CAS Web of Science® Google Scholar
Sugita H., Oshima K., Tamura M. & Deguchi Y. (1989) Bacterial flora of gastrointestine of freshwater fishes in river. Bulletin of Japanese Society Fisheries 49, 1387–1395.
10.2331/suisan.49.1387
Google Scholar
Sugita H., Miyajima C. & Deguchi Y. (1990) The vitamin B₁₂,- producing ability of the intestinal bacteria isolated from tilapia and channel catfish. Nippon Suisan Gakkaishi 56, 701.
10.2331/suisan.56.701
Web of Science® Google Scholar
Sugita H., Miyajima C. & Deguchi Y. (1991a) Vitamin B₁₂– producing ability of the intestinal microflora of freshwater fish. Aquaculture 92, 267–276.
10.1016/0044-8486(91)90028-6
CAS Web of Science® Google Scholar
Sugita H., Takahashi J., Miyajima C. & Deguchi Y. (1991b) Vitamin B₁₂, producing ability of the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Agricultural Biology and Chemistry 55, 893–894.
10.1271/bbb1961.55.893
CAS Web of Science® Google Scholar
Sugita H., Takahashi J., Miyajima C. & Deguchi Y. (1992) Effect of culture conditions on the growth and vit. B₁₂ productivity of anaerobic intestinal bacteria isolated from freshwater fishes. Bulletin of College of Agriculture and Veterinary Medicine, Nihon University 9, 122–127.
Google Scholar
Sugita H., Nakamura T., Tanaka K. & Deguchi Y. (1994) Identification of Aeromonas species isolated from freshwater fish with the microplate hybridization method. Applied and Environmental Microbiology 60, 3036–3038.
10.1128/aem.60.8.3036-3038.1994
CAS PubMed Web of Science® Google Scholar
Sugita H., Shibuyu K., Shimooka H. & Deguchi Y. (1996) Antibacterial activities of intestinal bacteria in freshwater cultured fish. Aquaculture 145, 195–203.
10.1016/S0044-8486(96)01319-1
Web of Science® Google Scholar
Sugita H., Matsuo N., Hirose Y., Iwato M. & Deguchi Y. (1997) Vibrio sp. strain NM 10 with an inhibitory effect against Pasteurella piscicida from the intestine of Japanese coastal fish. Applied Environmental Microbiology 63, 4986–4989.
CAS PubMed Web of Science® Google Scholar
Sugita H., Ishigaki T., Iwai D., Suzuki Y., Okano R., Matsuura S., Asfie M., Aono E. & Deguchi Y. (1998) Antibacterial abilities of intestinal bacteria from three coastal fishes. Suisanzoshoku 46, 563–568.
Google Scholar
Sugita H., Hirose Y., Matsuo N. & Deguchi Y. (1998) Production of the antibacterial substance by Bacillus sp. strain NM 12, an intestinal bacterium of Japanese coastal fish. Aquaculture 165, 269–280.
10.1016/S0044-8486(98)00267-1
CAS Web of Science® Google Scholar
Sugita H., Okano R., Suzuki Y., Iwai D., Mizukami M., Akiyama N. & Matusuura S. (2002) Antibacterial abilities of intestinal bacteria from larvae and juvenile Japanese flounder against fish pathogens. Fisheries Science 68, 1004–1011.
10.1046/j.1444-2906.2002.00525.x
CAS Web of Science® Google Scholar
Sugita H., Kurosaki M., Okamura T., Yamamoto S. & Tsuchiya C. (2005) The culturability of intestinal bacteria of Japanese coastal fish. Fisheries Science 71, 956–958.
10.1111/j.1444-2906.2005.01050.x
CAS Web of Science® Google Scholar
Sun Y., Yang H., Ling Z., Chang J. & Ye J. (2009) Gut microbiota of fast and slow growing grouper Epinephelus coioides. African Journal of Microbiology Research 3, 713–720.
Web of Science® Google Scholar
Syvokiene J. (1989) Simbiontnoe Pishchevarenie u Gidrobiontov Inasekomykh (Symbiotic Digestion in Hydrobionts and Insects), Mokslas, Vilnius, Lithuania.
Google Scholar
Syvokiene J. & Mickeniene L. (2002) Change in the intestinal microflora of molluscs from the Neris river depending on pollution. Acta Zoologica Lituanica 12, 76–81.
10.1080/13921657.2002.10512490
Google Scholar
Teitelbaum J.E. & Walker W.A. (2002) Nutritional impact of pre - and probiotics as protective gastrointestinal organisms. Annual Review of Nutrition 22, 107–138.
10.1146/annurev.nutr.22.110901.145412
CAS PubMed Web of Science® Google Scholar
Temmerman R., Huys G. & Swings J. (2004) Identification of lactic acid bacteria: culture-dependent and culture independent methods. Trends in Food Science and Technology 15, 348–359.
10.1016/j.tifs.2003.12.007
CAS Web of Science® Google Scholar
Teply L.J., Krehi W.A. & Elvehjem C.A. (1947) The intestinal synthesis of niacin and folic acid in the rat. American Journal of Physiology 148, 91–97.
CAS PubMed Web of Science® Google Scholar
Teshima S. & Kashiwada K. (1967) Studies on the production of B vitamins by intestinal bacteria of fish. 3. Isolation of vitamin B₁₂ synthesizing bacteria and their bacteriological properties. Bulletin of the Japanese Society of Scientific Fisheries 33, 979–983.
10.2331/suisan.33.979
Google Scholar
Torrecillas S., Makol A., Caballero M.J., Montero D., Robaina L., Real F., Sweetman J., Tort L. & Izquierdo M.S. (2007) Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish and Shellfish Immunology 23, 969–981.
10.1016/j.fsi.2007.03.007
CAS PubMed Web of Science® Google Scholar
Trust T. (1975) Facultative anaerobic bacteria in the digestive tract of Chinook salmon (Oncorhtbchus keta) maintained in freshwater under defined cultured conditions. Applied Microbiology 29, 663–668.
PubMed Web of Science® Google Scholar
Trust T.J. & Sparrow R.A.H. (1974) The bacterial flora in the alimentary tract of freshwater salmonid fishes. Canadian Journal of Microbiology 20, 1219–1228.
10.1139/m74-188
PubMed Web of Science® Google Scholar
Trust T.J., Bull L.M., Currie B.R. & Buckley J.T. (1979) Obligate anaerobic bacteria in the gastrointestinal microflora of the grass carp (Ctenopharyngodon idella), gold fish (Carassius auratus) and rainbow trout (Salmo gairdneri). Journal of Fishery Research Board Canada 36, 1174–1179.
10.1139/f79-169
Web of Science® Google Scholar
Tsuchiya C., Sakata T. & Sugita H. (2008) Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Letters in Applied Microbiology 46, 43–48.
10.1111/j.1472-765X.2007.02258.x
CAS PubMed Web of Science® Google Scholar
Tuohy K.M., Rouzaud G.C.M., Bruck W.M. & Gibson G.R. (2005) Modulation of the human gut microflora towards improved health using prebiotics – assessment of efficacy. Current Pharmaceutical Design 11, 75–90.
10.2174/1381612053382331
CAS PubMed Web of Science® Google Scholar
Tytler P. & Blaxter J.S. (1988) Drinking in the yolk-sac stage larvae of the halibut, Hippoglossus hippoglossus (L.). Journal of Fish Biology 32, 493–494.
10.1111/j.1095-8649.1988.tb05388.x
Web of Science® Google Scholar
Uchii K., Matsui K., Yonekura R., Tani K., Kenzaka T., Nasu M. & Kawabata Z. (2006) Genetic and physiological characterization of the intestinal bacterial microbiota of Bluegill (Lepomis macrochirus) with three different feeding habits. Microbial Ecology 51, 277–283.
10.1007/s00248-006-9018-z
CAS PubMed Web of Science® Google Scholar
Umesaki Y. & Setoyama H. (2000) Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes and Infection 2, 1343–1351.
10.1016/S1286-4579(00)01288-0
CAS PubMed Web of Science® Google Scholar
Uphill P.F., Jalob F. & Lall P. (1977) Vitamin B₁₂ production by gastrointestinal microflora of baboon and fed either a vitamin B₁₂ deficient diet or a diet supplemented with a vitamin B₁₂. Journal of Applied Bacteriology 43, 333–344.
10.1111/j.1365-2672.1977.tb00760.x
CAS PubMed Web of Science® Google Scholar
Vanhoutte T., Huys G., De Brandt E., Fahey J. & Swings J. (2005) Molecular monitoring and characterization of the faecal microbiota of healthy dogs during fructan supplementation. FEMS Microbiology Letters 249, 65–71.
10.1016/j.femsle.2005.06.003
CAS PubMed Web of Science® Google Scholar
Verner-Jeffreys D.W., Shields R.J., Bricknell I.R. & Birkbeck T.H. (2003) Changes in the gut-associated microflora during the development of Atlantic halibut (Hippoglossus hippoglossus L.) larvae in three British hatcheries. Aquaculture 219, 21–42.
10.1016/S0044-8486(02)00348-4
Web of Science® Google Scholar
Voveriene G., Mickeniene L. & Syvokiene J. (2002) Hydrocarbon-degrading bacteria in the digestive tract of fish, their abundance, species composition, and activity. Acta Zoologica Lituanica 12, 333–340.
10.1080/13921657.2002.10512520
Google Scholar
Walter J., Hertel C., Tannock G.W., Lis C.M., Munro K. & Hammes W.P. (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 67, 2578–2585.
10.1128/AEM.67.6.2578-2585.2001
CAS PubMed Web of Science® Google Scholar
Wang H., He M., Live P., Hu T. & Chen T. (1994) Study on the intestinal microflora of carp in freshwater cultured pond. Acta Hydrobiologica 18, 354–359.
Web of Science® Google Scholar
Ward N.L., Steven B., Penn K., Methe B.A. & Detrich W.H. III (2009) Characterization of the intestinal microbiota of two Antarctic notothenioid fish species. Extremophiles 13, 679–685.
10.1007/s00792-009-0252-4
PubMed Web of Science® Google Scholar
Westerdahl A., Olsson J., Kjelleberg S. & Conway P.T. (1991) Isolation and characterisation of turbot (Scophthalmus maximus) associated bacteria with inhibitory effects against Vibrio anguillarum. Applied and Environmental Microbiology 57, 2223–2228.
CAS PubMed Web of Science® Google Scholar
Westerdahl A., Olsson J.C., Conway P. & Kjellberg S. (1994) Characterisation of turbot (Scophthalmus maximus) associated bacteria with inhibitory effect against the fish pathogen Vibrio anguillarum. Acta Microbiology Immunology Hungerica 41, 403–409.
PubMed Google Scholar
White L.A., Newman M.C., Cromwell G.L. & Lindemann M.D. (2002) Brewers dried yeast as a source of mannan oligosaccharides for weanling pigs. Journal of Animal Science 80, 2619–2628.
CAS PubMed Web of Science® Google Scholar
Xu B., Wang Y., Li J. & Lin Q. (2009) Effect of prebiotic xylooligosaccharides on growth performances and digestive enzyme activities of allogynogenetic crucian carp (Carassius auratus gibelio). Fish Physiology and Biochemistry 35, 351–357.
10.1007/s10695-008-9248-8
CAS PubMed Web of Science® Google Scholar
Xu J., Bjursell M.K., Himrod J., Deng S., Carmichael L.K., Chiang H.C., Hooper L.V. & Gordon J.I. (2003) A genomic view of the human- Bacteroides thetaiotaomicron symbiosis. Science 299, 2074–2076.
10.1126/science.1080029
CAS PubMed Web of Science® Google Scholar
Yoshimizu M. & Kimura T. (1976) Study on the intestinal microflora of salmonids. Fish Pathology 10, 243–259.
10.3147/jsfp.10.243
Google Scholar
Yoshimizu M., Kimura T. & Sakai M. (1976) Studies of the intestinal microflora of salmonids. 1. The intestinal microflora of fish reared in fresh water and sea water. Bulletin of the Japanese Society of Scientific Fisheries 42, 91–99.
10.2331/suisan.42.91
Web of Science® Google Scholar
Yoshimizu M., Kimura T. & Sakai M. (1980) Microflora of the embryo and the fry of salmonids. Bulletin of the Japanese Society of Scientific Fisheries 46, 967–975.
10.2331/suisan.46.967
Web of Science® Google Scholar
Youssef H., E1-Timawy A.K. & Ahmed S. (1992) Role of aerobic intestinal pathogens of freshwater fish in transmission of human disease. Journal of Food Protection 55, 739–740.
10.4315/0362-028X-55.9.739
Web of Science® Google Scholar
Zaman Z. & Leong T.S. (1994) Intestinal distribution of a Caryophyllidae cestode, Lytocestus parvulus, furtado 1963, in Clarias batrachus (L.) from Malaysia. In: The Proceeding of the Third Asian Fisheries Forum, (ed. by L.M Chou, A.D. Munro, T.J. Lam, T.W. Chen, L.K.K. Cheong, J.K. Ding, K.K. Hooi, H.W. Khoo, V.P.E Phang, K.F Shim & C.H Tan), pp. 314–316. Asian Fisheries Society, Manila, Philippines.
Web of Science® Google Scholar
Zapata A. & Amemiya C.T. (2000) Phylogeny of lower vertebrates and their immunological structures. Origin and evolution of the vertebrate immune system. Current Topics in Microbiology and Immunology 248, 67–107.
10.1007/978-3-642-59674-2_5
CAS PubMed Web of Science® Google Scholar
Zapata A., Diez B., Cejalvo T., Gutierrez-de F.C. & Cortes A. (2006) Ontogeny of the immune system of fish. Fish and Shellfish Immunology 20, 126–136.
10.1016/j.fsi.2004.09.005
CAS PubMed Web of Science® Google Scholar
Zhou X., Tian Z., Wang Y. & Li W. (2009) Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune response. Fish Physiology and Biochemistry, doi: DOI: 10.1007/s10695-009-9320-z.
10.1007/s10695-009-9320-z
PubMed Web of Science® Google Scholar

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Role of gastrointestinal microbiota in fish

Abstract

Introduction

Development and establishment of GI microbiota of fish

Factors affecting the establishment of GI microbiota

Microbial composition in the GI tract of fish

Role of GI microbiota in fish: gnotobiotic approaches

Role of GI microbiota in immunity

Role of GI microbiota in nutrition

Role of GI microbiota in disease outbreak

Role of GI microbiota in fish health management

Manipulation of GI microbiota in fish

Probiotics concept

Prebiotics concept

Conclusion

Acknowledgment

References

Citing Literature

References

Information

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Role of gastrointestinal microbiota in fish

Abstract

Introduction

Development and establishment of GI microbiota of fish

Factors affecting the establishment of GI microbiota

Microbial composition in the GI tract of fish

Role of GI microbiota in fish: gnotobiotic approaches

Role of GI microbiota in immunity

Role of GI microbiota in nutrition

Role of GI microbiota in disease outbreak

Role of GI microbiota in fish health management

Manipulation of GI microbiota in fish

Probiotics concept

Prebiotics concept

Conclusion

Acknowledgment

References

Citing Literature

References

Related

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