Chapter 20
Gene Mining for Environmental Studies and Applications: Examples from Marine Organisms
Simon M. Dittami,
Thierry Tonon,
Simon M. Dittami
Sorbonne Universitées UPMC Univ Paris 06 UMR 8227, Integrative Biology of Marine Models Station Biologique de Roscoff CS 90074, F-29688, Roscoff cedex, France
Search for more papers by this authorThierry Tonon
CNRS UMR 8227, Integrative Biology of Marine Models Station Biologique de Roscoff CS 90074, F-29688, Roscoff cedex, France
Search for more papers by this authorSimon M. Dittami,
Thierry Tonon,
Simon M. Dittami
Sorbonne Universitées UPMC Univ Paris 06 UMR 8227, Integrative Biology of Marine Models Station Biologique de Roscoff CS 90074, F-29688, Roscoff cedex, France
Search for more papers by this authorThierry Tonon
CNRS UMR 8227, Integrative Biology of Marine Models Station Biologique de Roscoff CS 90074, F-29688, Roscoff cedex, France
Search for more papers by this authorBook Editor(s):Stéphane La Barre,
Jean-Michel Kornprobst,
Stéphane La Barre
Sorbonne Universités, UPMC Univ Paris 06, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
Search for more papers by this authorJean-Michel Kornprobst
Institut Mer et Littoral,Bâtiment Isomer, 2, rue de la Houssinière, 44322 Nantes, BP 92208,Cedex 3, France
Search for more papers by this authorSummary
In this chapter, some of the most common techniques used to generate genomic and transcriptomic data, that is, sequence and gene expression information, are reviewed. Examples are then given as to how these data can be exploited to understand the physiology of marine organisms. Emphasis is placed on studies conducted to gain insights on the response of corals to climate change (temperature and acidification), and on toxin production by dinoflagellates (dinotoxins). Finally, attention is focused on molecular biomonitoring techniques, and how sequence information can be used to assess the quality of food and the environment for the benefit of humans. The integration of genomic and transcriptomic data with other levels of analysis will lay the ground for a better understanding and exploitation of the potential of marine systems.
References
- Ahn, S., Kulis David, M., Erdner, D.L., Anderson Donald, M., and Walt, D.R. (2006) Fiber-optic microarray for simultaneous detection of multiple harmful algal bloom species. Appl. Environ. Microbiol., 72, 5742–5749.
- Amann, R. and Ludwig, W. (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol. Rev., 24, 555–565.
-
R. Andersen (ed.)
(2005)
Algal Culturing Techniques,
Elsevier,
Amsterdam.
10.1016/B978-012088426-1/50007-X Google Scholar
- Andree, K.B., Fernández-Tejedor, M., Elandaloussi, L.M., Quijano-Scheggia, S., Sampedro, N., Garcés, E., Camp, J., and Diogène, J. (2011) Quantitative PCR coupled with melt curve analysis for detection of selected pseudo-Nitzschia spp. (Bacillariophyceae) from the Northwestern Mediterranean sea. Appl. Environ. Microbiol., 77, 1651–1659.
- Apt, K.E., Clendennen, S.K., Powers, D.A., and Grossman, A.R. (1995) The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera . Mol. Gen. Genet., 246, 455–464.
- Barshis, D.J., Ladner, J.T., Oliver, T.A., Seneca, F.O., Traylor-Knowles, N., and Palumbi, S.R. (2013) Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. USA, 110, 1387–1392.
- Bay, L.K., Ulstrup, K.E., Nielsen, H.B., Jarmer, H., Goffard, N., Willis, B.L., Miller, David J., and Van Oppen, M.J.H. (2009) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora . Mol. Ecol., 18, 3062–3075.
- Bellantuono, A.J., Granados-Cifuentes, C., Miller, D.J., Hoegh-Guldberg, O., and Rodriguez-Lanetty, M. (2012) Coral thermal tolerance: tuning gene expression to resist thermal stress. PloS ONE, 7, e50685.
- Bowers, H.A., Tengs, T., Glasgow, H.B., Burkholder, J.M., Rublee, P.A., and Oldach, D.W. (2000) Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl. Environ. Microbiol., 66, 4641–4648.
- Bowers, H.A., Tomas, C., Tengs, Torstein, Kempton, J.W., Lewitus, A.J., and Oldach David, W. (2006) Raphidophyceae [Chadefaud ex Silva] systematics and rapid identification: sequence analyses and real-time PCR assays. J. Phycol., 42, 1333–1348.
- Bustin, S.A. (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol., 25, 169–193.
- Camacho, F.G., Rodríguez, J.G., Mirón, A.S., García, M.C.C., Belarbi, E.H., Chisti, Y., and Grima, E.M. (2007) Biotechnological significance of toxic marine dinoflagellates. Biotechnol. Adv., 25, 176–194.
- Campbell, B.J., Yu, L., Heidelberg, J.F., and Kirchman, D.L. (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc. Natl Acad. Sci. USA, 108, 12776–12781.
- Casper, E.T., Paul, J.H., Smith, M.C., and Gray, M. (2004) Detection and quantification of the red tide dinoflagellate Karenia brevis by real-time nucleic acid sequence-based amplification. Appl. Environ. Microbiol., 70, 4727–4732.
- Castiglioni, B., Rizzi, E., Frosini, A., Sivonen, K., Rajaniemi, P., Rantala, A., Mugnai, M.A., Ventura, S., Wilmotte, A., Boutte, C., Grubisic, S., Balthasart, P., Consolandi, C., Bordoni, R., Mezzelani, A., Battaglia, C., and De Bellis, G. (2004) Development of a universal microarray based on the ligation detection reaction and 16S rRNA gene polymorphism to target diversity of cyanobacteria. Appl. Environ. Microbiol., 70, 7161–7172.
- Chakravorty, S., Helb, D., Burday, M., Connell, N., and Alland, D. (2007) A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods, 69, 330–339.
- Cock, J.M., Sterck, L., Rouzé, P., Scornet, D., Allen, A.E. et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465, 617–621.
- Coley, P.D., Bryant, J.P., and Chapin, F.S. (1985) Resource availability and plant antiherbivore defense. Science, 230, 895–899.
- Collén, J., Porcel, B., Carré, W., Ball, S.G., Chaparro, C. et al. (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl Acad. Sci. USA, 110, 5247–5252.
- Coyne, K.J., Handy, S.M., Demir, E., Whereat, E.B., Hutchins, D.A., Portune, K.J., Doblin, M.A., and Cary, S.C. (2005) Improved quantitative real-time PCR assays for enumeration of harmful algal species in field samples using an exogenous DNA reference standard. Limnol. Oceanogr.: Methods, 3, 381–391.
- DeSalvo, M.K., Voolstra, C.R., Sunagawa, S., Schwarz, J.A., Stillman, J.H., Coffroth, M.A., Szmant, A.M., and Medina, M. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata . Mol. Ecol., 17, 3952–3971.
- Dittami, S.M. and Edvardsen, B. (2012) Culture conditions influence cellular RNA content in ichthyotoxic flagellates of the genus Pseudochattonella (Dictyochophyceae). J. Phycol., 48, 1050–1055.
- Dittami, S.M. and Edvardsen, B. (2013) GPR-Analyzer: a simple tool for quantitative analysis of hierarchical multispecies microarrays. Environ. Sci. Pollut. R., 20, 6808–6815.
- Dittami, S.M., Hostyeva, V., Egge, E.S., Kegel, J.U., Eikrem, W., and Edvardsen, B. (2013) Seasonal dynamics of harmful algae in outer Oslofjorden monitored by microarray, qPCR, and microscopy. Environ. Sci. Pollut. R., 20, 6719–6732.
- Dittami, S.M., Riisberg, I., and Edvardsen, B. (2013) Molecular probes for the detection and identification of ichthyotoxic marine microalgae of the genus Pseudochattonella (Dictyochophyceae, Ochrophyta). Environ. Sci. Pollut. R., 20, 6824–6837.
- Drake, J.L., Mass, T., Haramaty, L., Zelzion, E., Bhattacharya, D., and Falkowski, Paul G. (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata . Proc. Natl Acad. Sci. USA, 110, 3788–3793.
- Ebenezer, V., Medlin, L.K., and Ki, J.-S. (2012) Molecular detection, quantification, and diversity evaluation of microalgae. Mar. Biotechnol., 14, 129–142.
- Edge, S.E., Shearer, T.L., Morgan, M.B., and Snell, T.W. (2013) Sub-lethal coral stress: Detecting molecular responses of coral populations to environmental conditions over space and time. Aquat. Toxicol., 128–129, 135–146.
- Edge, Sara E., Morgan, Michael B., Gleason, D.F., and Snell Terry, W. (2005) Development of a coral cDNA array to examine gene expression profiles in Montastraea faveolata exposed to environmental stress. Mar. Pollut. Bull., 51, 507–523.
- Edvardsen, B., Dittami, S.M., Groben, R., Brubak, S., Escalera, L., Rodríguez, F., Reguera, B., Chen, J., and Medlin, L.K. (2013) Molecular probes and microarrays for the detection of toxic algae in the genera Dinophysis and Phalacroma (Dinophyta). Environ. Sci. Pollut. R., 20, 6733–6750.
- Eichholz, K., Beszteri, B., and John, U. (2012) Putative monofunctional type I polyketide synthase units: a dinoflagellate-specific feature? PloS ONE, 7, e48624.
- Emblem, A., Karlsen, B.O., Evertsen, J., Miller, D.J., Moum, T., and Johansen, S.D. (2012) Mitogenome polymorphism in a single branch sample revealed by SOLiD deep sequencing of the Lophelia pertusa coral genome. Gene, 506, 344–349.
- Eppard, M. and Rhiel, E. (1998) The genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family. Mol. Gen. Genet., 260, 335–345.
- Errera, R.M., Bourdelais, A., Drennan, M.A., Dodd, E.B., Henrichs, D.W., and Campbell, L. (2010) Variation in brevetoxin and brevenal content among clonal cultures of Karenia brevis may influence bloom toxicity. Toxicon, 55, 195–203.
- Errera, R.M. and Campbell, L. (2011) Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis . Proc. Natl Acad. Sci. USA, 108, 10597–10601.
- Fabris, M., Matthijs, M., Rombauts, S., Vyverman, W., Goossens, A., and Baart, G.J.E. (2012) The metabolic blueprint of Phaeodactylum tricornutum reveals a eukaryotic Entner-Doudoroff glycolytic pathway. Plant J., 70, 1004–1014.
- Falkowski, Paul G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O., and Taylor, F.J.R. (2004) The evolution of modern eukaryotic phytoplankton. Science, 305, 354–360.
- El Fantroussi, S., Urakawa, H., Bernhard, A.E., Kelly, J.J., Noble, P.A., Smidt, H., Yershov, G.M., and Stahl, D.A. (2003) Direct profiling of environmental microbial populations by thermal dissociation analysis of native rRNAs hybridized to oligonucleotide microarrays. Appl. Environ. Microbiol., 69, 2377–2382.
- Fegatella, F., Lim, J., Kjelleberg, S., and Cavicchioli, R. (1998) Implications of rRNA operon copy number and ribosome content in the marine oligotrophic ultramicrobacterium Sphingomonas sp. strain RB2256. Appl. Environ. Microbiol., 64, 4433–4438.
- Forêt, S., Kassahn, K.S., Grasso, L.C., Hayward, D.C., Iguchi, A., Ball, E.E., and Miller, D.J. (2007) Genomic and microarray approaches to coral reef conservation biology. Coral Reefs, 26, 475–486.
- Fu, F.-X., Place, A.R., Garcia, N.S., and Hutchins, D.A. (2010) CO2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum . Aquat. Microb. Ecol., 59, 55–65.
- Fu, F.-X., Tatters, A., and Hutchins, D. (2012) Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser., 470, 207–233.
- Gallardo-Rodríguez, J., Sánchez-Mirón, A., García-Camacho, F., López-Rosales, L., Chisti, Y., and Molina-Grima, E. (2012) Bioactives from microalgal dinoflagellates. Biotechnol. Adv., 30, 1673–1684.
- Galluzzi, L., Penna, A., Bertozzini, E., Giacobbe, M.-G., Vila, M., Garcés, E., Prioli, S., and Magnani, M. (2005) Development of a qualitative PCR method for the Alexandrium spp. (Dinophyceae) detection in contaminated mussels (Mytilus galloprovincialis). Harmful Algae, 4, 973–983.
- Gescher, C., Metfies, K., Frickenhaus, S., Knefelkamp, B., Wiltshire, K.H., and Medlin, L.K. (2008) Feasibility of assessing the community composition of prasinophytes at the Helgoland Roads sampling site with a DNA microarray. Appl. Environ. Microbiol., 74, 5305–5316.
- Gescher, C., Metfies, K., and Medlin, L.K. (2008) The ALEX CHIP - development of a DNA chip for identification and monitoring of Alexandrium . Harmful Algae, 7, 485–494.
- Glöckner, F.O., Kube, M., Bauer, M., Teeling, H., Lombardot, T., Ludwig, W., Gade, D., Beck, A., Borzym, K., Heitmann, K., Rabus, R., Schlesner, H., Amann, R., and Reinhardt, R. (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl Acad. Sci. USA, 100, 8298–8303.
- Gobet, A., Böer, S.I., Huse, S.M., Van Beusekom, J.E.E., Quince, C., Sogin, M.L., Boetius, A., and Ramette, A. (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J., 6, 542–553.
- Góngora-Castillo, E. and Buell, C.R. (2013) Bioinformatics challenges in de novo transcriptome assembly using short read sequences in the absence of a reference genome sequence. Nat. Prod. Rep., 30, 490–500.
- Granados-Cifuentes, C., Bellantuono, A.J., Ridgway, T., Hoegh-Guldberg, O., and Rodriguez-Lanetty, M. (2013) High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity. BMC Genomics, 14, 228.
- Grasso, Lauretta C., Maindonald, J., Rudd, S., Hayward David, C., Saint, R., Miller, David J., and Ball Eldon, E. (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics, 9, 540.
- Gray, M., Wawrik, B., Paul, J., and Casper, E.T. (2003) Molecular detection and quantitation of the red tide dinoflagellate Karenia brevis in the marine environment. Appl. Environ. Microbiol., 69, 5726–5730.
- Groben, R., John, U., Eller, G., Lange, M., and Medlin, L.K. (2004) Using fluorescently-labelled rRNA probes for hierarchical estimation of phytoplankton diversity – a mini-review. Nova Hedwigia, 79, 313–320.
- Groben, R. and Medlin, L.K. (2005) In situ hybridization of phytoplankton using fluorescently labeled rRNA probes. Methods Enzymol., 395, 299–310.
- Grossman, A.R. (2007) In the grip of algal genomics. Adv. Exp. Med. Biol., 616, 54–76.
- Grzebyk, D. (2003) Effects of salinity and two coastal waters on the growth and toxin content of the dinoflagellate Alexandrium minutum . J. Plankton Res., 25, 1185–1199.
- Hackett, J.D., Wisecaver, J.H., Brosnahan, M.L., Kulis, D.M., Anderson Donald, M., Bhattacharya, D., Plumley, F.G., and Erdner, D.L. (2013) Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol. Biol. Evol., 30, 70–78.
- Hamasaki, K., Hori, M., Tokimitsu, S., Toda, T., and Taguchi, S. (2001) Variability in toxicity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, western Japan, as a reflection of changing environmental conditions. J. Plankton Res., 23, 271–278.
- Hardison, D.R., Sunda, W.G., Shea, D., and Litaker, R.W. (2013) Increased toxicity of Karenia brevis during phosphate limited growth: ecological and evolutionary implications. PLoS ONE, 8, e58545.
- Hardison, D.R., Sunda, W.G., Wayne Litaker, R., Shea, D., and Tester, P.A. (2012) Nitrogen limitation increases brevetoxins in Karenia brevis (Dinophyceae): implications for bloom toxicity. J. Phycol., 48, 844–858.
- Harlow, L.D., Koutoulis, A., and Hallegraeff, G.M. (2007) S-adenosylmethionine synthetase genes from eleven marine dinoflagellates. Phycologia, 46, 46–53.
- Ho, P., Kong, K.F., Chan, Y.H., Tsang, J.S.H., and Wong, J.T.Y. (2007) An unusual S-adenosylmethionine synthetase gene from dinoflagellate is methylated. BMC Mol. Biol., 8, 87.
- Holland, P.M. (1991) Detection of specific polymerase chain reaction product by utilizing the 5′-3′ exonuclease activity of Thermus aquaticus DNA polymerase. Proc. Natl Acad. Sci. USA, 88, 7276–7280.
- Humbert, J.F., Quiblier, C., and Gugger, M. (2010) Molecular approaches for monitoring potentially toxic marine and freshwater phytoplankton species. Anal. Bioanal. Chem., 397, 1723–1732.
- Iverson, V., Morris, R.M., Frazar, C.D., Berthiaume, C.T., Morales, R.L., and Armbrust, E.V. (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science, 335, 587–590.
- Jaeckisch, N., Yang, I., Wohlrab, S., Glöckner, G., Kroymann, J., Vogel, H., Cembella, A., and John, U. (2011) Comparative genomic and transcriptomic characterization of the toxigenic marine dinoflagellate Alexandrium ostenfeldii . PloS ONE, 6, e28012.
- Joint, I., Mühling, M., and Querellou, J. (2010) Culturing marine bacteria – an essential prerequisite for biodiscovery. Microbial. Biotechnol., 3, 564–575.
- Kamikawa, R., Nagai, S., Hosoi-Tanabe, S., Itakura, S., Yamaguchi, M., Uchida, Y., Baba, T., and Sako, Y. (2007) Application of real-time PCR assay for detection and quantification of Alexandrium tamarense and Alexandrium catenella cysts from marine sediments. Harmful Algae, 6, 413–420.
- Kegel, J.U., Del Amo, Y., and Medlin, L.K. (2013) Introduction to project MIDTAL: its methods and samples from Arcachon Bay, France. Environ. Sci. Pollut. R., 20, 6690–6704.
- Kellmann, R., Mihali, T.K., Jeon, Y.J., Pickford, R., Pomati, F., and Neilan Brett, A. (2008) Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl. Environ. Microbiol., 74, 4044–4053.
- Kellmann, R., Stüken, A., Orr, R.J.S., Svendsen, H.M., and Jakobsen, K.S. (2010) Biosynthesis and molecular genetics of polyketides in marine dinoflagellates. Marine Drugs, 8, 1011–1048.
- Klinge, S., Voigts-Hoffmann, F., Leibundgut, M., and Ban, N. (2012) Atomic structures of the eukaryotic ribosome. Trends Biochem. Sci., 37, 189–198.
- Krumholz, E.W., Yang, H., Weisenhorn, P., Henry, C.S., and Libourel, I.G.L. (2012) Genome-wide metabolic network reconstruction of the picoalga Ostreococcus . J. Exp. Bot., 63, 2353–2362.
- Kubota, T., Iinuma, Y., and Kobayashi, J. (2006) Cloning of polyketide synthase genes from amphidinolide-producing dinoflagellate Amphidinium sp. Biol. Pharm. Bull., 29, 1314–1318.
- Lami, R., Ghiglione, J.-F., Desdevises, Y., West, N.J., and Lebaron, P. (2009) Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA-16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat. Microb. Ecol., 54, 199–210.
- Lange, M., Guillou, L., Vaulot, D., Simon, N., Amann, R., Ludwig, W., and Medlin, L.K. (1996) Identification of the class Prymnesiophyceae and the genus Phaeocystis with ribosomal RNA-targeted nucleic acid probes detected by flow cytometry. J. Phycol., 32, 858–868.
- Leblanc, C., Falciatore, A., Watanabe, M., and Bowler, C. (1999) Semi-quantitative RT-PCR analysis of photoregulated gene expression in marine diatoms. Plant Mol. Biol., 40, 1031–1044.
- Lewis, J., Medlin, L.K., and Raine, R. (2012) MIDTAL (Microarrays for the Detection of Toxic Algae): A Protocol for a Successful Microarray Hybridisation and Analysis (eds J. Lewis, L.K. Medlin, and R. Raine), Koeltz Scientific Books, Koenigstein, Germany.
- Lidie, K.B., Ryan, J.C., Barbier, M., and Van Dolah, F.M. (2005) Gene expression in Florida red tide dinoflagellate Karenia brevis: analysis of an expressed sequence tag library and development of DNA microarray. Mar. Biotechnol., 7, 481–493.
- Lim, P.-T. and Ogata, T. (2005) Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon, 45, 699–710.
- Lin, S. (2006) Low abundance distribution of Pfiesteria piscicida in Pacific and Western Atlantic as detected by mtDNA-18S rDNA real-time polymerase chain reaction. J. Plankton Res., 28, 667–681.
- Lin, S. (2011) Genomic understanding of dinoflagellates. Res. Microbiol., 162, 551–569.
- Liu, L., Li, Yinhu, Li, S., Hu, N., He, Y., Pong, R., Lin, D., Lu, L., Law, M. (2012) Comparison of next-generation sequencing systems. J. Biomed. Biotechnol., 2012, 251364.
- Ten Lohuis, M.R. and Miller, D.J. (1998) Genetic transformation of dinoflagellates (Amphidinium and Symbiodinium): expression of GUS in microalgae using heterologous promoter constructs. Plant J., 13, 427–435.
- López-Legentil, S., Song, B., DeTure, M., and Baden, D.G. (2010) Characterization and localization of a hybrid non-ribosomal peptide synthetase and polyketide synthase gene from the toxic dinoflagellate Karenia brevis . Mar. Biotechnol., 12, 32–41.
- Loy, A., Lehner, A., Lee, N., Adamczyk, J., Meier, H., Ernst, J., Schleifer, K.-H., and Wagner, M. (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl. Environ. Microbiol., 68, 5064–5081.
- Magaña, H.A. and Villareal, T.A. (2006) The effect of environmental factors on the growth rate of Karenia brevis (Davis) G. Hansen and Moestrup. Harmful Algae, 5, 192–198.
- Maier Brown, A.F., Dortch, Q., Van Dolah, F.M., Leighfield, T.A., Morrison, W., Thessen, A.E., Steidinger, K., Richardson, B., Moncreiff, C.A., and Pennock, J.R. (2006) Effect of salinity on the distribution, growth, and toxicity of Karenia spp. Harmful Algae, 5, 199–212.
- Marcelino, L.A., Backman, V., Donaldson, A., Steadman, C., Thompson, J.R., Preheim, S.P., Lien, C., Lim, E., Veneziano, D., and Polz, M.F. (2006) Accurately quantifying low-abundant targets amid similar sequences by revealing hidden correlations in oligonucleotide microarray data. Proc. Natl Acad. Sci. USA, 103, 13629–13634.
- Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader, J.S. et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.
- Metfies, K., Borsutzki, P., Gescher, C., Medlin, L.K., and Frickenhaus, S. (2008) PhylochipAnalyser - a program for analysing hierarchical probe sets. Mol. Ecol. Resour., 8, 99–102.
- Meyer, E., Aglyamova, G.V., and Matz, M.V. (2011) Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol. Ecol., 20, 3599–3616.
- Meyer, E., Aglyamova Galina, V., Wang, S., Buchanan-Carter, J., Abrego, D., Colbourne, J.K., Willis, B.L., and Matz Mikhail, V. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics, 10, 219.
- Miller, D.J., Ball, E., Forêt, S., and Satoh, N. (2011) Coral genomics and transcriptomics – Ushering in a new era in coral biology. J. Exp. Mar. Biol. Ecol., 408, 114–119.
- Monod, J. (1949) The growth of bacterial cultures. Annu. Rev. Microbiol., 3, 371–394.
- Monroe, E.A. and Van Dolah, F.M. (2008) The toxic dinoflagellate Karenia brevis encodes novel type I-like polyketide synthases containing discrete catalytic domains. Protist, 159, 471–482.
- Monroe, E.A., Johnson, J.G., Wang, Z., Pierce, R.K., and Van Dolah, F.M. (2010) Characterization and expression of nuclear-encoded polyketide synthases in the brevetoxin-producing dinoflagellate Karenia brevis . J. Phycol., 46, 541–552.
-
Morgan, M.B.,
Edge, S.E., and
Snell, T.W.
(2005)
Profiling differential gene expression of corals along a transect of waters adjacent to the Bermuda municipal dump.
Mar. Pollut. Bull.,
51,
524–533.
10.1016/j.marpolbul.2005.09.023 Google Scholar
- Moustafa, A., Evans, A.N., Kulis, D.M., Hackett, J.D., Erdner, D.L., Anderson, D.M., and Bhattacharya, D. (2010) Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PloS ONE, 5, e9688.
- Moustafa, A., Loram, J.E., Hackett, J.D., Anderson, D.M., Plumley, F.G., and Bhattacharya, D. (2009) Origin of saxitoxin biosynthetic genes in cyanobacteria. PloS ONE, 4, e5758.
- Moya, A., Huisman, L., Ball, E.E., Hayward, D.C., Grasso, L.C., Chua, C.M., Woo, H.N., Gattuso, J.-P., Forêt, S., and Miller, D.J. (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol. Ecol., 21, 2440–2454.
- Murray, S.A., Garby, T., Hoppenrath, M., and Neilan, B.A. (2012) Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata). PloS ONE, 7, e38253.
- Murray, S.A., Wiese, M., Stüken, A., Brett, S., Kellmann, R., Hallegraeff, G., and Neilan, B.A. (2011) SxtA-Based quantitative molecular assay to identify daxitoxin-producing harmful algal blooms in marine waters. Appl. Environ. Microbiol., 77, 7050–7057.
- Orr, R.J.S., Murray, S.A., Stüken, A., Rhodes, L., and Jakobsen, K.S. (2012) When naked became armored: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS ONE, 7, e50004.
- Orr, R.J.S., Stüken, A., Murray, S.A., and Jakobsen, K.S. (2013) Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: the Second “core” gene, sxtG. Appl. Environ. Microbiol., 79, 2128–2136.
- Owens, T.G., Falkowski, P.G., and Whitledge, T.E. (1980) Diel periodicity in cellular chlorophyll content in marine diatoms. Mar. Biol., 59, 71–77.
- Park, T.-G., Park, G.-H., Park, Y.-T., Kang, Y.-S., Bae, H.-M., Kim, C.-H., Jeong, H.-J., and Lee, Y. (2009) Identification of the dinoflagellate community during Cochlodinium polykrikoides (Dinophyceae) blooms using amplified rDNA melting curve analysis and real-time PCR probes. Harmful Algae, 8, 430–440.
- Park, T.-G., Park, Y.-T., and Lee, Y. (2009) Development of a SYTO9 based real-time PCR probe for detection and quantification of toxic dinoflagellate Karlodinium veneficum (Dinophyceae) in environmental samples. Phycologia, 48, 32–43.
- Park, T.-G., De Salas, M.F., Bolch, C.J.S., and Hallegraeff, G.M. (2007) Development of a real-time PCR probe for quantification of the heterotrophic dinoflagellate Cryptoperidiniopsis brodyi (Dinophyceae) in environmental samples. Appl. Environ. Microbiol., 73, 2552–2560.
- Parker, M.S., Mock, T., and Armbrust, E.V. (2008) Genomic insights into marine microalgae. Annu. Rev. Genet., 42, 619–645.
- Penna, A., Bertozzini, E., Battocchi, C., Galluzzi, L., Giacobbe, M.G., Vila, M., Garces, E., Luglie, A., and Magnani, M. (2007) Monitoring of HAB species in the Mediterranean Sea through molecular methods. J. Plankton Res., 29, 19–38.
- Peplies, J., Lau, S.C.K., Pernthaler, J., Amann, R., and Glöckner, F.O. (2004) Application and validation of DNA microarrays for the 16S rRNA-based analysis of marine bacterioplankton. Environ. Microbiol., 6, 638–645.
- Peter, I.S., Faure, E., and Davidson, E.H. (2012) Predictive computation of genomic logic processing functions in embryonic development. Proc. Natl Acad. Sci. USA, 109, 16434–16442.
- Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
- Polato, N.R., Altman, N.S., and Baums, I.B. (2013) Variation in the transcriptional response of threatened coral larvae to elevated temperatures. Mol. Ecol., 22, 1366–1382.
- Polato, N.R., Vera, J.C., and Baums, I.B. (2011) Gene discovery in the threatened elkhorn coral: 454 sequencing of the Acropora palmata transcriptome. PloS ONE, 6, e28634.
- Rein, K.S. and Snyder, R.V. (2006) The biosynthesis of polyketide metabolites by dinoflagellates. Adv. Appl. Microbiol., 59, 93–125.
- Rodriguez-Lanetty, M., Harii, S., and Hoegh-Guldberg, O. (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol. Ecol., 18, 5101–5114.
- Rossini, G.P. and Hess, P. (2010) Phycotoxins: chemistry, mechanisms of action and shellfish poisoning. Experientia Supplementa, 100, 65–122.
- Salcedo, T., Upadhyay, R.J., Nagasaki, K., and Bhattacharya, D. (2012) Dozens of toxin-related genes are expressed in a nontoxic strain of the dinoflagellate Heterocapsa circularisquama . Mol. Biol. Evol., 29, 1503–1506.
- Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463–5467.
- Schwarz, J.A., Brokstein, P.B., Voolstra, C., Terry, A.Y., Manohar, C.F., Miller, D.J., Szmant Alina, M., Coffroth, M.A., and Medina, M. (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata . BMC Genomics, 9, 97.
- Sethi, A.J., Angerer, R.C., and Angerer, L.M. (2009) Gene regulatory network interactions in sea urchin endomesoderm induction. PLoS Biol., 7, e1000029.
- Shen, B. (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr. Opin. Chem. Biol., 7, 285–295.
- Shimizu, Y. (1996) Microalgal metabolites: a new perspective. Annu. Rev. Microbiol., 50, 431–465.
- Shinzato, C., Shoguchi, E., Kawashima, T., Hamada, M., Hisata, K., Tanaka, M., Fujie, M., Fujiwara, M., Koyanagi, R., Ikuta, T., Fujiyama, A., Miller, D.J., and Satoh, N. (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature, 476, 320–323.
- Snyder, R.V., Gibbs, P.D.L., Palacios, A., Abiy, L., Dickey, R., Lopez, J.V., and Rein, K.S. (2003) Polyketide synthase genes from marine dinoflagellates. Mar. Biotechnol., 5, 1–12.
- Snyder, R.V., Guerrero, M.A., Sinigalliano, C.D., Winshell, J., Perez, R., Lopez Jose, V., and Rein, K.S. (2005) Localization of polyketide synthase encoding genes to the toxic dinoflagellate Karenia brevis . Phytochemistry, 66, 1767–1780.
- Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Avery, K.B., Tignor, M., and Miller, H.L. (2007) Climate Change 2007 - The Physical Science Basis, Cambridge University Press, Cambridge.
- Stüken, A., Orr, R.J.S., Kellmann, R., Murray, S.A., Neilan Brett, A., and Jakobsen, K.S. (2011) Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PloS ONE, 6, e20096.
- Sun, J., Chen, Q., Lun, J.C.Y., Xu, J., and Qiu, J.-W. (2013) PcarnBase: Development of a transcriptomic database for the brain coral Platygyra carnosus . Mar. Biotechnol., 15, 244–251.
- Sunda, W.G. and Huntsman, S.A. (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature, 390, 389–392.
- Tang, J.-Q., Li, T., Yang, W.-D., Liu, J.-S., and Li, H.-Y. (2009) Cloning and expression analysis of PKS gene in Prorocentrum lima . Acta Ecologica Sinica, 29, 2383–2390.
- Taroncher-Oldenburg, G., Kulis, D.M., and Anderson, D.M. (1997) Toxin variability during the cell cycle of the dinoflagellate Alexandrium fundyense . Limnol. Oceanogr., 42, 1178–1188.
- Teeling, H., Fuchs, B.M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C.M., Kassabgy, M., Huang, S., Mann, A.J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F.D., Callies, U., Gerdts, G., Wichels, A., Wiltshire, K.H., Glöckner, F.O., Schweder, T., and Amann, R. (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336, 608–611.
- Tonon, T., Harvey, D., Larson, T.R., and Graham, I.A. (2003) Identification of a very long chain polyunsaturated fatty acid Delta4-desaturase from the microalga Pavlova lutheri . FEBS Lett., 553, 440–444.
- Tonon, T., Harvey, D., Qing, R., Li, Yi., Larson, T.R., and Graham, I.A. (2004) Identification of a fatty acid Δ11-desaturase from the microalga Thalassiosira pseudonana . FEBS Lett., 563, 28–34.
- Touzet, N., Keady, E., Raine, R., and Maher, M. (2009) Evaluation of taxa-specific real-time PCR, whole-cell FISH and morphotaxonomy analyses for the detection and quantification of the toxic microalgae Alexandrium minutum (Dinophyceae), Global Clade ribotype. FEMS Microbiol. Ecol., 67, 329–341.
- Traylor-Knowles, N., Granger, B.R., Lubinski, T.J., Parikh, J.R., Garamszegi, S., Xia, Y., Marto, J.A., Kaufman, L., and Finnerty, J.R. (2011) Production of a reference transcriptome and transcriptomic database (PocilloporaBase) for the cauliflower coral, Pocillopora damicornis . BMC Genomics, 12, 585.
- Tyagi, S. and Kramer, F.R. (1996) Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol., 14, 303–308.
- Ulrich, R.M., Casper, E.T., Campbell, L., Richardson, B., Heil, C.A., and Paul, J.H. (2010) Detection and quantification of Karenia mikimotoi using real-time nucleic acid sequence-based amplification with internal control RNA (IC-NASBA). Harmful Algae, 9, 116–122.
- Venn, A.A., Loram, J.E., and Douglas, A.E. (2008) Photosynthetic symbioses in animals. J. Exp. Bot., 59, 1069–1080.
- Wang, D.-Z., Gao, Y., Lin, L., and Hong, H.-S. (2013) Comparative proteomic analysis reveals proteins putatively involved in toxin biosynthesis in the marine dinoflagellate Alexandrium catenella . Mar. Drugs, 11, 213–232.
- Wang, Zhong, Gerstein, M., and Snyder, M. (2009) RNAseq: a revolutionary tool for transcriptomics. Nat. Rev. Genet., 10, 57–63.
- Wuyts, J., Van de Peer, Y., Winkelmans, T., and De Wachter, R. (2002) The European database on small subunit ribosomal RNA. Nucleic Acids Res., 30, 183–185.
- Yang, I., John, U., Beszteri, S., Glöckner, G., Krock, B., Goesmann, A., and Cembella, A.D. (2010) Comparative gene expression in toxic versus non-toxic strains of the marine dinoflagellate Alexandrium minutum . BMC Genomics, 11, 248.
- Yang, I., Selander, E., Pavia, H., and John, U. (2011) Grazer-induced toxin formation in dinoflagellates: a transcriptomic model study. Eur. J. Phycol., 46, 66–73.
- Zhang, F., Ma, L., Xu, Z., Zheng, J., Shi, Y., Lu, Y., and Miao, Y. (2009) Sensitive and rapid detection of Karenia mikimotoi (Dinophyceae) by loop-mediated isothermal amplification. Harmful Algae, 8, 839–842.
