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Distribution of High Bacterial Taxa Across the Chronosequence of Two Alpine Glacier Forelands

  • Environmental Microbiology
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Abstract

Little is known about the changes in abundance of microbial taxa in relation to the chronosequence of receding glaciers. This study investigated how the abundances of ten bacterial phyla or classes varied along successional gradients in two glaciers, Ödenwinkelkees and Rotmoosferner, in the central Alps. Quantitative PCR was used to estimate the abundance of the different bacterial taxa in extended glacier chronosequences, including 10- to 160-year-old successional stages, the surface of the glacier, and a fully established soil. Actinobacteria (15–30%) was the dominant group within the chronosequences. Several taxa showed significant differences in the number of taxa-specific 16S rRNA gene copies per nanogram of DNA and/or in the ratio of taxa-specific to the total bacterial 16S rRNA gene copies (i.e., the relative abundance of the different taxa within the bacterial community) between the established soils or the glacier surface and the 10- to 160-year-old successional stages. A significantly higher proportion of Βetaproteobacteria (20%) was observed on the surface of both glaciers. However, no differences were observed between the 10- to 160-year-old successional stages in the number of taxa-specific 16S rRNA gene copies per nanogram of DNA or in the ratio of taxa-specific to the total bacterial 16S rRNA gene copies for the different taxa. Nevertheless, when the relative abundance data from all the studied taxa were combined and analyzed altogether, most of the sites could be distinguished from one other. This indicates that the overall composition of the bacterial community was more affected than the abundance of the targeted taxa by changes in environmental conditions along the chronosequences.

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References

  1. Acosta-Martinez V, Dowd S, Sun Y, Allen V (2009) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  Google Scholar 

  2. Bardgett RD, Richter A, Bol R, Garnett MH, Bäumler R, Xu X, Lopez-Capel E, Manning DAC, Hobbs PJ, Hartley IR, Wanek W (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3:487–490

    Article  PubMed  Google Scholar 

  3. Bormann B, Sidle R (1990) Changes in productivity and distribution of nutrients in a chronosequence at glacier Bay National Park, Alaska. J Ecol 78:561–578

    Article  Google Scholar 

  4. Bru D, Martin-Laurent F, Philippot L (2008) Quantification of the detrimental effect of a single primer-template mismatch by real-time PCR using the 16S rRNA gene as an example. Appl Environ Microbiol 74:1660–1663

    Article  CAS  PubMed  Google Scholar 

  5. Cébron A, Norini M-P, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHD[alpha]) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Meth 73:148–159

    Article  Google Scholar 

  6. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175

    Article  Google Scholar 

  7. Cheng SM, Foght JM (2007) Cultivation-independent and -dependent characterization of bacteria resident beneath John Evans Glacier. FEMS Microbiol Ecol 59:318–330

    Article  CAS  PubMed  Google Scholar 

  8. Crocker RL, Major J (1955) Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J Ecol 43:427–448

    Article  Google Scholar 

  9. Deiglmayr K, Philippot L, Tscherko D, Kandeler E (2006) Microbial succession of nitrate-reducing bacteria in the rhizosphere of Poa alpina across a glacier foreland in the Central Alps. Environ Microbiol 8:1600–1612

    Article  CAS  PubMed  Google Scholar 

  10. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  11. Fierrer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    Article  Google Scholar 

  12. Foght J, Aislabie J, Turner S, Brown CE, Ryburn J, Saul DJ, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two Southern Hemisphere glaciers. Microb Ecol 47:329–340

    Article  CAS  PubMed  Google Scholar 

  13. Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc Natl Acad Sci USA 105:17842–17847

    Article  CAS  PubMed  Google Scholar 

  14. Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundance of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189

    Article  CAS  PubMed  Google Scholar 

  15. Huggett RJ (1998) Soil chronosequences, soil development, and soil evolution: a critical review. Catena 32:155–172

    Article  Google Scholar 

  16. Insam H, Haselwandter K (1989) Metabolic quotient of the soil microflora in relation to plant succession. Oecologia 79:174–178

    Article  Google Scholar 

  17. Jangid K, Williams MA, Franzluebbers AJ, Sanderlin JS, Reeves JH, Jenkins MB, Endale DM, Coleman DC, Whitman WB (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40:2843–2853

    Article  CAS  Google Scholar 

  18. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK and nosZ genes of denitrifying bacteria during primary successions of glacier foreland. Appl Environ Microbiol 72:5957–5962

    Article  CAS  PubMed  Google Scholar 

  21. Kaufmann R (2001) Invertebrate succession on an alpine glacier foreland. Ecology 82:2261–2278

    Article  Google Scholar 

  22. Kielak A, Pijl A, Veen JV, Kowalchuk G (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382

    Article  CAS  PubMed  Google Scholar 

  23. Klappenbach JA, Saxman PR, Cole JR, Schmidt TM (2001) rrndb: the Ribosomal RNA Operon Copy Number Database. Nucleic Acid Res 29:181–184

    Article  CAS  PubMed  Google Scholar 

  24. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  PubMed  Google Scholar 

  25. Liu YQ, Yao TD, Kang SC, Jiao NZ, Zeng YH, Huang SJ, Luo TW (2007) Microbial community structure in major habitats above 6000 m on Mount Everest. Chin Sci Bull 52:2350–2357

    Article  Google Scholar 

  26. Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon JC, Soulas G, Catroux G (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol 67:2354–2359

    Article  CAS  PubMed  Google Scholar 

  27. Matthews JA (1992) The ecology of recently-deglaciated terrain. A geoecological approach to glacier forelands and primary succession. Cambridge University Press, Cambridge

    Google Scholar 

  28. Mühling M, Woolven-Allen J, Murrell JC, Joint I (2008) Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J 2(4):379–392

    Article  PubMed  Google Scholar 

  29. Nemergut DR, Andersen S, Cleveland C, Martin A, Miller A, Seimon A, Schmidt S (2007) Microbial community succession in an unvegetated recently deglaciated soil. Microb Ecol 53:110–122

    Article  PubMed  Google Scholar 

  30. Nicol G, Tscherko D, Embley T, Prosser J (2005) Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7:337–347

    Article  CAS  PubMed  Google Scholar 

  31. Noll M, Wellinger M (2008) Changes of the soil ecosystem along a receding glacier: testing the correlation between environmental factors and bacterial community structure. Soil Biol Biochem 40:2611–2619

    Article  CAS  Google Scholar 

  32. Ohtonen R, Hannu F, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246

    Article  Google Scholar 

  33. Philippot L, Andersson SGE, Battin TJ, Prosser J, Schimel J, Whitman W, Hallin S (2010) The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8:523–529

    Article  CAS  PubMed  Google Scholar 

  34. Philippot L, Bru D, Saby NPA, Cuhel J, Arrouays D, Simek M, Hallin S (2009) Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches of the 16S rRNA bacterial tree. Environ Microbiol 11:3096–3104

    Article  CAS  PubMed  Google Scholar 

  35. Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 106:19964–19969

    CAS  PubMed  Google Scholar 

  36. Roesch L, Fulthorpe RR, Riva A, Casella G, Hadwin A, Kent A, Daroub S, Camargo F, Farmerie W, Triplett E (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290

    CAS  PubMed  Google Scholar 

  37. Sattin SR, Cleveland CC, Hood E, Reed SC, King AJ, Schmidt SK, Robeson MS, Ascarrunz N, Nemergut DR (2009) Functional shifts in unvegetated, perhumid, recently-deglaciated soil do not correlate with shifts in soil bacterial community composition. J Microbiol 47:673–681

    Article  PubMed  Google Scholar 

  38. Schipper LA, Degens BP, Sparling GP, Duncan LC (2001) Changes in microbial heterotrophic diversity along five plant successional sequences. Soil Biol Biochem 33:2093–2103

    Article  CAS  Google Scholar 

  39. Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC, Martin AM (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc Royal Soc B-Biol Sci 275:2793–2802

    Article  CAS  Google Scholar 

  40. Schütte UME, Abdo Z, Bent SJ, Williams CJ, Schneider GM, Solheim B, Forney LJ (2009) Bacterial succession in a glacier foreland of the High Artic. ISME J 3:1258–1268

    Article  PubMed  Google Scholar 

  41. Sigler W, Crivii S, Zeyer J (2002) Bacterial succession in glacial forefield soils characterized by community structure, activity and opportunistic growth dynamics. Microb Ecol 44:306–316

    Article  CAS  PubMed  Google Scholar 

  42. Sigler W, Zeyer J (2002) Microbial diversity and activity along the forefields of two receding glaciers. Microb Ecol 43:397–407

    Article  CAS  PubMed  Google Scholar 

  43. Skidmore M, Anderson SP, Sharp M, Foght J, Lanoil BD (2005) Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl Environ Microbiol 71:6986–6997

    Article  CAS  PubMed  Google Scholar 

  44. Sparks DL (1996) Methods of soil analysis. Part 3. Chemical methods (Soil Science Society of America Book Series, No. 5). Soil Science Society of America, Inc., Madison, p 1309

    Google Scholar 

  45. Tscherko D, Hammesfahr U, Marx M-C, Kandeler E (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36:1685–1698

    Article  CAS  Google Scholar 

  46. Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E (2003) Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur J Soil Sci 54:685–696

    Article  Google Scholar 

  47. Tscherko D, Hammesfahr U, Zeltner G, Kandeler E, Böcker R (2005) Soil microflora function and composition in recently deglaciated alpine terrain: impact of early and late coloniser plants. Basic Appl Ecol 6:367–383

    Article  CAS  Google Scholar 

  48. Weiher E, Keddy PA (1999) Relative abundance and evenness patterns along diversity and biomass gradients. Oikos 87:355–361

    Article  Google Scholar 

  49. Whittaker RJ (1993) Plant population patterns in a glacier foreland succession: pioneer herbs and later-colonizing shrubs. Ecography 16:117–136

    Article  Google Scholar 

  50. Youssef NH, Elshahed NS (2009) Diversity rankings among baterial lineages in soil. ISME J 3:305–313

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank the Sequencing and Genotyping Service (SSG) in Dijon. Many thanks to Christoph Schweizer, Graeme Nicol, Anne-Maree Dean, and Jim Prosser who developed the sampling design of this study together with us and who supported us during soil sampling in Austria. We also acknowledge the technical assistance of Elke Feiertag and Cornelia Ruf in the laboratory.

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Authors and Affiliations

  1. INRA, UMR 1229, Soil and Environmental Microbiology, 17 rue Sully, 21065, Dijon Cedex, France

    Laurent Philippot & David Bru

  2. Université de Bourgogne, 21065, Dijon Cedex, France

    Laurent Philippot & David Bru

  3. Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, 70593, Stuttgart, Germany

    Dagmar Tscherko & Ellen Kandeler

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  1. Laurent Philippot
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Correspondence to Laurent Philippot.

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Philippot, L., Tscherko, D., Bru, D. et al. Distribution of High Bacterial Taxa Across the Chronosequence of Two Alpine Glacier Forelands. Microb Ecol 61, 303–312 (2011). https://doi.org/10.1007/s00248-010-9754-y

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