Soil characteristics more strongly influence soil bacterial communities than land-use type
Corresponding Author
Eiko E. Kuramae
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Ecological Science, Free University Amsterdam, Amsterdam, The Netherlands
Correspondence: Eiko E. Kuramae, Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands. Tel.: +31 317 473 502; fax: +31 317 473 675; e-mail: [email protected]Search for more papers by this authorEtienne Yergeau
Biotechnology Research Institute, National Research Council of Canada, Montréal, QC, Canada
Search for more papers by this authorLina C. Wong
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Search for more papers by this authorAgata S. Pijl
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Search for more papers by this authorJohannes A. van Veen
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Biology, Leiden University, Leiden, The Netherlands
Search for more papers by this authorGeorge A. Kowalchuk
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Ecological Science, Free University Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorCorresponding Author
Eiko E. Kuramae
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Ecological Science, Free University Amsterdam, Amsterdam, The Netherlands
Correspondence: Eiko E. Kuramae, Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands. Tel.: +31 317 473 502; fax: +31 317 473 675; e-mail: [email protected]Search for more papers by this authorEtienne Yergeau
Biotechnology Research Institute, National Research Council of Canada, Montréal, QC, Canada
Search for more papers by this authorLina C. Wong
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Search for more papers by this authorAgata S. Pijl
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Search for more papers by this authorJohannes A. van Veen
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Biology, Leiden University, Leiden, The Netherlands
Search for more papers by this authorGeorge A. Kowalchuk
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
Institute of Ecological Science, Free University Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorAbstract
To gain insight into the factors driving the structure of bacterial communities in soil, we applied real-time PCR, PCR-denaturing gradient gel electrophoreses, and phylogenetic microarray approaches targeting the 16S rRNA gene across a range of different land usages in the Netherlands. We observed that the main differences in the bacterial communities were not related to land-use type, but rather to soil factors. An exception was the bacterial community of pine forest soils (PFS), which was clearly different from all other sites. PFS had lowest bacterial abundance, lowest numbers of operational taxonomic units (OTUs), lowest soil pH, and highest C : N ratios. C : N ratio strongly influenced bacterial community structure and was the main factor separating PFS from other fields. For the sites other than PFS, phosphate was the most important factor explaining the differences in bacterial communities across fields. Firmicutes were the most dominant group in almost all fields, except in PFS and deciduous forest soils (DFS). In PFS, Alphaproteobacteria was most represented, while in DFS, Firmicutes and Gammaproteobacteria were both highly represented. Interestingly, Bacillii and Clostridium OTUs correlated with pH and phosphate, which might explain their high abundance across many of the Dutch soils. Numerous bacterial groups were highly correlated with specific soil factors, suggesting that they might be useful as indicators of soil status.
Supporting Information
Filename | Description |
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fem1192-sup-0001-FigureS1.pptapplication/mspowerpoint, 97 KB | Fig. S1. Map of sampling sites with different land use. |
fem1192-sup-0002-FigureS2.docWord document, 36 KB | Fig. S2. Schematic representation of soil sampling per field. |
fem1192-sup-0003-FigureS3.pptapplication/mspowerpoint, 465 KB | Fig. S3. Bacterial PCR-DGGE band patterns between replicates (A, B, C, D, E) and between fields (F1, F2, F3, F4, F7, F8, F9, F10, F11). |
fem1192-sup-0004-FigureS4.pptapplication/mspowerpoint, 137.5 KB | Fig. S4. Canonical correspondence analysis of normalized intensities given in PhyloChips, sampling sites, and significant soil factors (red arrows) for 25 soils sampled across the Netherlands. |
fem1192-sup-0005-TableS1.docWord document, 36 KB | Table S1. Pearson's correlation between bacterial and fungal abundance quantified by real-time PCR and soil physical and chemical factors. |
fem1192-sup-0006-TableS2.docWord document, 33 KB | Table S2. Pearson's correlation between total numbers of OTUs given in the PhyloChips and soil physicochemical factors and fungal abundance of 25 different fields. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Ahmad N, Johri S, Abdin M & Qazi G (2009) Molecular characterization of bacterial population in the forest soil of Kashmir, India. World J Microbiol Biotechnol 25: 107–113.
- Aislabie J, Jordan S, Ayton J, Klassen JL, Barker GM & Turner S (2009) Bacterial diversity associated with ornithogenic soil of the Ross Sea region, Antarctica. Can J Microbiol 55: 21–36.
- Baker KL, Langenheder S, Nicol GW, Ricketts D, Killham K, Campbell CD & Prosser JI (2009) Environmental and spatial characterisation of bacterial community composition in soil to inform sampling strategies. Soil Biol Biochem 41: 2292–2298.
- Benjamini Y & Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289–300.
- Brodie EL, DeSantis TZ, Joyner DC et al. (2006) Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72: 6288–6298.
- Caracciolo AB, Grenni P, Ciccoli R, Di Landa G & Cremisini C (2005) Simazine biodegradation in soil: analysis of bacterial community structure by in situ hybridization. Pest Manag Sci 61: 863–869.
- Chatzinotas A, Sandaa RA, Schonhuber W et al. (1998) Analysis of broad-scale differences in microbial community composition of two pristine forest soils. Syst Appl Microbiol 21: 579–587.
- DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM & Andersen GL (2007) High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol 53: 371–383.
- Doran JW & Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15: 3–11.
- Enwall K, Nyberg K, Bertilsson S, Cederlund H, Stenstrom J & Hallin S (2007) Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol Biochem 39: 106–115.
- Felske A, Wolterink A, Van Lis R & Akkermans ADL (1998) Phylogeny of the main bacterial 16S rRNA sequences in Drentse A grassland soils (The Netherlands). Appl Environ Microbiol 64: 871–879.
- Felske A, Wolterink A, Van Lis R, De Vos WM & Akkermans ADL (2000) Response of a soil bacterial community to grassland succession as monitored by 16S rRNA levels of the predominant ribotypes. Appl Environ Microbiol 66: 3998–4003.
- Fields MW, Bagwell CE, Carroll SL et al. (2006) Phylogenetic and functional biomakers as indicators of bacterial community responses to mixed-waste contamination. Environ Sci Technol 40: 2601–2607.
- Fierer N & Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103: 626–631.
- Fierer N, Jackson JA, Vilgalys R & Jackson RB (2006) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71: 4117–4120.
- Filip Z (2002) International approach to assessing soil quality by ecologically-related biological parameters. Agric Ecosyst Environ 88: 169–174.
- Haichar FE, Marol C, Berge O et al. (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2: 1221–1230.
- Hansel CM, Fendorf S, Jardine PM & Francis CA (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74: 1620–1633.
- Jangid K, Williams MA, Franzluebbers AJ et al. (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40: 2843–2853.
- Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72: 1719–1728.
- Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R & Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3: 442–453.
- Kennedy N, Connolly J & Clipson N (2005) Impact of lime, nitrogen and plant species on fungal community structure in grassland microcosms. Environ Microbiol 7: 780–788.
- Kobabe S, Wagner D & Pfeiffer EM (2004) Characterisation of microbial community composition of a Siberian tundra soil by fluorescence in situ hybridisation. FEMS Microbiol Ecol 50: 13–23.
- Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL & van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81: 509–520.
- Kuramae EE, Gamper HA, Yergeau E et al. (2010) Microbial secondary succession in a chronosequence of chalk grasslands. ISME J 4: 711–715.
- Kuramae EE, Gamper H, van Veen JA & Kowalchuk GA (2011) Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol Ecol 77: 285–294.
- Lauber CL, Strickland MS, Bradford MA & Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40: 2407–2415.
- Lauber CL, Hamady M, Knight R & Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community composition at the continental scale. Appl Environ Microbiol 75: 5111–5120.
- Lueders T, Wagner B, Claus P & Friedrich MW (2004) Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol 6: 60–72.
- Marschner P, Yang CH, Lieberei R & Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33: 1437–1445.
- Nemergut DR, Townsend AR, Sattin SR et al. (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10: 3093–3105.
- Percent SF, Frischer ME, Vescio PA et al. (2008) Bacterial community structure of acid-impacted lakes: what controls diversity? Appl Environ Microbiol 74: 1856–1868.
- Pretty JN & Shah P (1997) Making soil and water conservation sustainable: from coercion and control to partnerships and participation. Land Degrad Dev 8: 39–58.
- Schutter ME, Sandeno JM & Dick RP (2001) Seasonal, soil type, and alternative management influences on microbial communities of vegetable cropping systems. Biol Fertil Soils 34: 397–410.
- Stein S, Selesi D, Schilling R, Pattis I, Schmid M & Hartmann A (2005) Microbial activity and bacterial composition of H-2-treated soils with net CO2 fixation. Soil Biol Biochem 37: 1938–1945.
- ter Braak CJF & Šmilauer P (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, NY.
- van Bruchem J, Schiere H & van Keulen H (1999) Dairy farming in the Netherlands in transition towards more efficient nutrient use. Livest Prod Sci 61: 145–153.
- Weinert N, Piceno Y, Ding G et al. (2011) Phylochip hybridization uncovered an enormous bacterial diversity in the rhizozphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol Ecol 75: 497–506.
- Wu T, Chellemi DO, Graham JH, Martin KJ & Rosskopf EN (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55: 293–310.
- Yergeau E, Bokhorst S, Huiskes AHL, Boschker HTS, Aerts R & Kowalchuk GA (2007) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59: 436–451.
- Yergeau E, Schoondermark-Stolk SA, Brodie EL et al. (2009) Environmental microarray analyses of Antarctic soil microbial communities. ISME J 3: 340–351.
- Zarda B, Hahn D, Chatzinotas A, Schonhuber W, Neef A, Amann RI & Zeyer J (1997) Analysis of bacterial community structure in bulk soil by in situ hybridization. Arch Microbiol 168: 185–192.
- Zhong WH, Gu T, Wang W, Zhang B, Lin XG, Huang QR & Shen WS (2010) The effects of mineral fertilizer and organic manure on soil microbial community and diversity. Plant Soil 326: 511–522.