Skip to main content

Advertisement

SpringerLink
Log in

Microbial Community Succession in an Unvegetated, Recently Deglaciated Soil

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Primary succession is a fundamental process in macroecosystems; however, if and how soil development influences microbial community structure is poorly understood. Thus, we investigated changes in the bacterial community along a chronosequence of three unvegetated, early successional soils (∼20-year age gradient) from a receding glacier in southeastern Peru using molecular phylogenetic techniques. We found that evenness, phylogenetic diversity, and the number of phylotypes were lowest in the youngest soils, increased in the intermediate aged soils, and plateaued in the oldest soils. This increase in diversity was commensurate with an increase in the number of sequences related to common soil bacteria in the older soils, including members of the divisions Acidobacteria, Bacteroidetes, and Verrucomicrobia. Sequences related to the Comamonadaceae clade of the Betaproteobacteria were dominant in the youngest soil, decreased in abundance in the intermediate age soil, and were not detected in the oldest soil. These sequences are closely related to culturable heterotrophs from rock and ice environments, suggesting that they originated from organisms living within or below the glacier. Sequences related to a variety of nitrogen (N)-fixing clades within the Cyanobacteria were abundant along the chronosequence, comprising 6–40% of phylotypes along the age gradient. Although there was no obvious change in the overall abundance of cyanobacterial sequences along the chronosequence, there was a dramatic shift in the abundance of specific cyanobacterial phylotypes, with the intermediate aged soils containing the greatest diversity of these sequences. Most soil biogeochemical characteristics showed little change along this ∼20-year soil age gradient; however, soil N pools significantly increased with soil age, perhaps as a result of the activity of the N-fixing Cyanobacteria. Our results suggest that, like macrobial communities, soil microbial communities are structured by substrate age, and that they, too, undergo predictable changes through time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410

    Article  PubMed  CAS  Google Scholar 

  2. Amann, RI, Ludwig, W, Schleifer, KH (1995) Phylogenetic identification and in-situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143–169

    PubMed  CAS  Google Scholar 

  3. Andren, O, Brussaard, L, Clarholm, M (1999) Soil organism influence on ecosystem-level processes bypassing the ecological hierarchy? Appl Soil Ecol 11: 177–188

    Article  Google Scholar 

  4. Battin, TJ, Wille, A, Sattler, B, Psenner, R (2001) Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microbiol 67: 799–807

    Article  PubMed  CAS  Google Scholar 

  5. Bormann, BT, Sidle, RC (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 

  6. Carrillo-Castaneda, G, Munoz, JJ, Peralta-Videa, JR, Gomez, E, Tiemannb, KJ, Duarte-Gardea, M, Gardea-Torresdey, JL (2002) Alfalfa growth promotion by bacteria grown under iron limiting conditions. Adv Environ Res 6: 391–399

    Article  Google Scholar 

  7. Chadwick, OA, Derry, LA, Vitousek, PM, Huebert, BJ, Hedin, LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397: 491–497

    Article  CAS  Google Scholar 

  8. 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 

  9. Clements, FE (1928) Plant Succession and Indicators: A Definitive Edition of Plant Succession and Plant Indicators. HW Wilson, New York

    Google Scholar 

  10. Cole, JR, Chai, B, Marsh, TL, Farris, RJ, Wang, Q, Kulam, SA, Chandra, S, McGarrell, DM, Schmidt, TM, Garrity, GM, Tiedje, JM (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442–443

    Article  PubMed  CAS  Google Scholar 

  11. Cooper, WS (1923) The recent ecological history of Glacier Bay, Alaska: II. The present vegetation cycle. Ecology 4: 223–246

    Article  Google Scholar 

  12. 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 

  13. Fastie, CL (1995) Causes and ecosystem consequences of multiple pathways of primary succession at Glacier Bay, Alaska. Ecology 76: 1899–1916

    Article  Google Scholar 

  14. Finlay, BJ, Maberly, SC, Cooper, JI (1997) Microbial diversity and ecosystem function. Oikos 80: 209–213

    Article  Google Scholar 

  15. Garreaud, RD, Munoz, R (2004) The diurnal cycle in circulation and cloudiness over the subtropical southeast Pacific: a modeling study. J Climate 17: 1699–1710

    Article  Google Scholar 

  16. Gleason, HA (1927) Further views on the succession concept. Ecology 8: 299–326

    Article  Google Scholar 

  17. Gordon, DA, Priscu, J, Giovannoni, S (2000) Origin and phylogeny of microbes living in permanent Antarctic lake ice. Microb Ecol 39: 197–202

    PubMed  Google Scholar 

  18. Hodkinson, ID, Coulson, SJ, Harrison, J, Webb, NR (2001) What a wonderful web they weave: spiders, nutrient capture and early ecosystem development in the high Arctic—some counter-intuitive ideas on community assembly. Oikos 95: 349–352

    Article  Google Scholar 

  19. Huber, T, Faulkner, G, Hugenholtz, P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Google Scholar 

  20. Huelsenbeck, JP, Ronquist, F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

    Article  PubMed  CAS  Google Scholar 

  21. Inagaki, F, Takai, K, Komatsu, T, Sakihama, Y, Inoue, A, Horikoshi, K (2002) Profile of microbial community structure and presence of endolithic microorganisms inside a deep-sea rock. Geomicrobiol J 19: 535–552

    Article  CAS  Google Scholar 

  22. Irgens, RL, Gosink, JJ, Staley, JT (1996) Polaromonas vacuolata gen nov, sp. nov, a psychrophilic, marine, gas vacuolate bacterium from Antarctica. Int J Syst Bacteriol 46: 822–826

    PubMed  CAS  Google Scholar 

  23. Jackson, CR, Harper, JP, Willoughby, D, Roden, EE, Churchill, PF (1997) A simple, efficient method for the separation of humic substances and DNA from environmental samples. Appl Environ Microbiol 63: 4993–4995

    PubMed  CAS  Google Scholar 

  24. Jumpponen, A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytol 158: 569–578

    Article  Google Scholar 

  25. Kemp, PF, Aller, JY (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol 47: 161–177

    Article  CAS  PubMed  Google Scholar 

  26. LaMontagne, MG, Schimel, JP, Holden, PA (2003) Comparison of subsurface and surface soil bacterial communities in California grassland as assessed by terminal restriction fragment length polymorphisms of PCR-amplified 16S rRNA genes. Microb Ecol 46: 216–227

    Article  PubMed  CAS  Google Scholar 

  27. Lane, DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt, E, Goodfellow, M (Eds.) Nucleic Acid Techniques in Bacterial Systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  28. Martin, AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68: 3673–3682

    Article  PubMed  CAS  Google Scholar 

  29. Martiny, AC, Jorgensen, TM, Albrechtsen, HJ, Arvin, E, Molin, S (2003) Long-term succession of structure and diversity of a biofilm formed in a model drinking water distribution system. Appl Environ Microbiol 69: 6899–6907

    Article  PubMed  CAS  Google Scholar 

  30. Matthews, JA (1992) The Ecology of Recently-Deglaciated Terrain: A Geoecological Approach to Glacier Forelands and Primary Succession. Cambridge University Press, Cambridge

    Google Scholar 

  31. More, MI, Herrick, JB, Silva, MC, Ghiorse, WC, Madsen, EL (1994) Quantitative cell-lysis of indigenous microorganisms and rapid extraction of microbial DNA from sediment. Appl Environ Microbiol 60: 1572–1580

    PubMed  CAS  Google Scholar 

  32. Nemergut, DR (2004) Evolution and ecology of high altitude soil microbial communities. Ph.D. dissertation, University of Colorado, Boulder, CO

  33. Nicol, GW, Tscherko, D, Embley, TM, Prosser, JI (2005) Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7: 337–347

    Article  PubMed  CAS  Google Scholar 

  34. Ohtonen, R, Fritze, H, 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 

  35. Pace, NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740

    Article  PubMed  CAS  Google Scholar 

  36. Park, IH, Ka, JO (2003) Isolation and characterization of 4-(2,4-dichlorophenoxy)butyric acid-degrading bacteria from agricultural soils. J Microbiol Biotechnol 13: 243–250

    CAS  Google Scholar 

  37. Priscu, JC, Adams, EE, Lyons, WB, Voytek, MA, Mogk, DW, Brown, RL, McKay, CP, Takacs, CD, Welch, KA, Wolf, CF, Kirshtein, JD, Avci, R (1999) Geomicrobiology of subglacial ice above Lake Vostok, Antarctica. Science 286: 2141–2144

    Article  PubMed  CAS  Google Scholar 

  38. Reese, CA, Liu, KB (2003) Pollen dispersal and deposition on the Quelccaya Ice Cap, Peru. Phys Geogr 23: 44–58

    Google Scholar 

  39. Roberts, GP, Ludden, PW (1992) Nitrogen fixation by photosynthetic bacteria. In: Stacey, G, Burris, RH, Evans, HJ (Eds.) Biological Nitrogen Fixation. Chapman & Hall, New York, pp 135–165

    Google Scholar 

  40. Sambrook, J, Russell, DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  41. 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 

  42. Schloss, PD, Handelsman, J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501–1506

    Article  PubMed  CAS  Google Scholar 

  43. Schloss, PD, Hay, AG, Wilson, DB, Gossett, JM, Walker, LP (2005) Quantifying bacterial population dynamics in compost using 16S rRNA gene probes. Appl Microbiol Biotechnol 66: 457–463

    Article  PubMed  CAS  Google Scholar 

  44. Schneider, S, Roessli, D, Excoffier, L. 2000. Arlequin: A software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva

  45. Shannon, DE, Weaver, W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana

    Google Scholar 

  46. Sheridan, PP, Miteva, VI, Brenchley, JE (2003) Phylogenetic analysis of anaerobic psychrophilic enrichment cultures obtained from a Greenland glacier ice core. Appl Environ Microbiol 69: 2153–2160

    Article  PubMed  CAS  Google Scholar 

  47. Sigler, WV, 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  49. 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  PubMed  CAS  Google Scholar 

  50. Staley, JT, Gosink, JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Annu Rev Microbiol 53: 189–215

    Article  PubMed  CAS  Google Scholar 

  51. Swofford, DL (2001) Phylogenetic Analysis Using Parsimony (*and Other Methods), 4th edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  52. Thompson, LG, Mosley-Thompson, E, Arnao, BM (1984) El-Nino southern oscillation events recorded in the stratigraphy of the tropical Quelccaya ice cap, Peru. Science 226: 50–53

    Article  PubMed  Google Scholar 

  53. Tiessen, H, Moir, JO (1993) Characterization of available P by sequential extraction. In: Carter, MR (Ed.) Soil Sampling and Methods of Analysis. Lewis Publishers, Boca Raton, pp 75–86

    Google Scholar 

  54. 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. Euro J of Soil Sci 54: 685–696

    Article  Google Scholar 

  55. Vitousek, PM (2004) Nutrient Cycling and Limitation: Hawai’i as a Model System. Princeton University Press, Princeton

    Google Scholar 

  56. Walker, LR, Clarkson, BD, Silvester, WB, Clarkson, BR (2003) Colonization dynamics and facilitative impacts of a nitrogen-fixing shrub in primary succession. J Veg Sci 14: 277–290

    Article  Google Scholar 

  57. Wardle, DA, Walker, LR, Bardgett, RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305: 509–513

    Article  PubMed  CAS  Google Scholar 

  58. Wen, AM, Fegan, M, Hayward, C, Chakraborty, S, Sly, LI (1999) Phylogenetic relationships among members of the Comamonadaceae, and description of Delftia acidovorans (den Dooren de Jong 1926 and Tamaoka et al. 1987) gen. nov., comb. nov. Int J Syst Bacteriol 49: 567–576

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Allen Meyer, Preston Sowell, and Julia Rosen for field assistance, Dan Liptzin for help with the biogeochemical analysis, Alex Blum for help with the XRD analysis, and Alan Townsend for valuable discussions. We also acknowledge the helpful suggestions of several thoughtful reviewers. Funding was provided from the NSF Microbial Observatories Program, grant MCB-0084223, and the Department of Ecology and Evolutionary Biology at the University of Colorado, Boulder, through the Marion and Gordon Alexander Memorial Scholarship for research in montane biology.

Author information

Authors and Affiliations

  1. INSTAAR, An Earth and Environmental Systems Institute, University of Colorado, Boulder, CO, 80309, USA

    Diana R. Nemergut, Suzanne P. Anderson, Cory C. Cleveland & Amy E. Miller

  2. Environmental Studies Program, University of Colorado, Boulder, CO, 80309, USA

    Diana R. Nemergut

  3. Department of Geography, University of Colorado, Boulder, CO, 80309, USA

    Suzanne P. Anderson

  4. Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Andrew P. Martin & Steven K. Schmidt

  5. National Park Service, Anchorage, AK, 99501, USA

    Amy E. Miller

  6. International Research Institute for Climate Prediction, Columbia University, Palisades, NY, 10964, USA

    Anton Seimon

Authors
  1. Diana R. Nemergut
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suzanne P. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cory C. Cleveland
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrew P. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amy E. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anton Seimon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Steven K. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana R. Nemergut.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nemergut, D.R., Anderson, S.P., Cleveland, C.C. et al. Microbial Community Succession in an Unvegetated, Recently Deglaciated Soil. Microb Ecol 53, 110–122 (2007). https://doi.org/10.1007/s00248-006-9144-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9144-7

Keywords

Search

Navigation