, Volume 11, Issue 7, pp 1157–1167 | Cite as

Fungal Taxa Target Different Carbon Sources in Forest Soil

  • China A. HansonEmail author
  • Steven D. Allison
  • Mark A. Bradford
  • Matthew D. Wallenstein
  • Kathleen K. Treseder


Soil microbes are among the most abundant and diverse organisms on Earth. Although microbial decomposers, particularly fungi, are important mediators of global carbon and nutrient cycling, the functional roles of specific taxa within natural environments remain unclear. We used a nucleotide-analog technique in soils from the Harvard Forest to characterize the fungal taxa that responded to the addition of five different carbon substrates—glycine, sucrose, cellulose, lignin, and tannin-protein. We show that fungal community structure and richness shift in response to different carbon sources, and we demonstrate that particular fungal taxa target different organic compounds within soil microcosms. Specifically, we identified eleven taxa that exhibited changes in relative abundances across substrate treatments. These results imply that niche partitioning through specialized resource use may be an important mechanism by which soil microbial diversity is maintained in ecosystems. Consequently, high microbial diversity may be necessary to sustain ecosystem processes and stability under global change.

Key words

fungi soil microbial diversity community structure soil carbon decomposition resource partitioning ecosystem function nucleotide analog 



We thank J. B. H. Martiny, J. T. Randerson, K. N. Suding, and J. Talbot for valuable discussions and comments on previous drafts of this manuscript. We also thank J. Borneman for assistance with molecular techniques, C. A. Davies for conducting substrate mineralization assays, A. Majumder for conducting qPCR assays, J. B. H. Martiny for statistical advice, J. M. Melillo for access to field sites, J. Mohan for sample collection, and members of the Treseder and Suding labs for discussions. This research was supported by the U.S. Department of Energy, Grant No. DE-FG02-04ER63893; and by the National Science Foundation, Grant No. DEB-0445458.

Supplementary material

10021_2008_9186_MOESM1_ESM.doc (66 kb)
(DOC 66 kb)


  1. Allison, S.D., Hanson, C.A., Treseder, K·K., 2007. Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biology & Biochemistry 39, 1878–1887.CrossRefGoogle Scholar
  2. Amarasekare, P., 2003. Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters 6, 1109–1122.CrossRefGoogle Scholar
  3. Bohannan, B.J.M., Kerr, B., Jessup, C.M., Hughes, J.B., Sandvik, G., 2002. Trade-offs and coexistence in microbial microcosms. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 81, 107–115.CrossRefGoogle Scholar
  4. Borneman, J., 1999. Culture-independent identification of microorganisms that respond to specified stimuli. Applied and Environmental Microbiology 65, 3398–3400.PubMedGoogle Scholar
  5. Borneman, J., Hartin, R.J., 2000. PCR primers that amplify fungal rRNA genes from environmental samples. Applied and Environmental Microbiology 66, 4356–4360.PubMedCrossRefGoogle Scholar
  6. Chao, A., 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265–270.Google Scholar
  7. Chapin, F·S., Walker, B·H., Hobbs, R.J., Hooper, D.U., Lawton, J.H., Sala, O.E., Tilman, D., 1997. Biotic control over the functioning of ecosystems. Science 277, 500–504.CrossRefGoogle Scholar
  8. Chase, J.M., Leibold, M.A., 2003. Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago.Google Scholar
  9. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., Thompson, J.D., 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research 31, 3497–3500.PubMedCrossRefGoogle Scholar
  10. Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–367.CrossRefGoogle Scholar
  11. Deacon, L.J., Pryce-Miller, E.J., Frankland, J.C., Bainbridge, B·W., Moore, P.D., Robinson, C·H., 2006. Diversity and function of decomposer fungi from a grassland soil. Soil Biology & Biochemistry 38, 7–20.CrossRefGoogle Scholar
  12. Felsenstein, J., 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genome Sciences, University of Washington, Seattle.Google Scholar
  13. Frankland, J.C., 1998. Fungal succession—unraveling the unpredictable. Mycological Research 102, 1–15.CrossRefGoogle Scholar
  14. Garrett, S.D., 1951. Ecological groups of soil fungi: a survey of substrate relationships. New Phytologist 50, 149–160.CrossRefGoogle Scholar
  15. Hagerman, A.E., Butler, L.G., 1978. Protein precipitation method for quantitative-determination of tannins. Journal of Agricultural and Food Chemistry 26, 809–812.CrossRefGoogle Scholar
  16. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
  17. Hawksworth, D.L., 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research 105, 1422–1432.CrossRefGoogle Scholar
  18. Hooper, D.U., Chapin, F·S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A.J., Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.CrossRefGoogle Scholar
  19. Kirk, T.K., Farrell, R.L., 1987. Enzymatic combustion—the microbial-degradation of lignin. Annual Review of Microbiology 41, 465–505.PubMedCrossRefGoogle Scholar
  20. Kjøller, A.H., Struwe, S., 2002. Fungal communities, succession, enzymes, and decomposition. In: Burns, R.G., Dick, R.P. (Eds.), Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York, NY, pp. 267–284.Google Scholar
  21. Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D., Wardle, D.A., 2001. Ecology-biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808.PubMedCrossRefGoogle Scholar
  22. Lynd, L.R., Weimer, P.J., van Zyl, W·H., Pretorius, I·S., 2002. Microbial cellulose utilization: fundamentals and biotechnology. Microbiology and Molecular Biology Reviews 66, 506–577.PubMedCrossRefGoogle Scholar
  23. Magurran, A.E., 1988. Ecological diversity and its measurement. Princeton University Press, Princeton NJGoogle Scholar
  24. Marschner, P., Rumberger, A., 2004. Rapid changes in the rhizosphere bacterial community structure during re-colonization of sterilized soil. Biology and Fertility of Soils 40, 1–6.CrossRefGoogle Scholar
  25. McCune, B., Grace, J.B., 2002. Analysis of ecological communities. MjM Software Design, Glendon Beach, OR.Google Scholar
  26. McKane, R.B., Johnson, L.C., Shaver, G.R., Nadelhoffer, K.J., Rastetter, E.B., Fry, B., Giblin, A.E., Kielland, K., Kwiatkowski, B.L., Laundre, J.A., Murray, G., 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415, 68–71.PubMedCrossRefGoogle Scholar
  27. Nannipieri, P., Ascher, J., Ceccherini, M.T., Landi, L., Pietramellara, G., Renella, G., 2003. Microbial diversity and soil functions. Eur J Soil Sci 54, 655–670.CrossRefGoogle Scholar
  28. Peterjohn, W.T., Melillo, J.M., Steudler, P.A., Newkirk, K.M., Bowles, F·P., Aber, J.D., 1994. Responses of trace gas fluxes and N availability to experimentally elevated soil temperatures. Ecological Applications 4, 617–625.CrossRefGoogle Scholar
  29. R Development Core Team, 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  30. Robinson, C·H., Miller, E.J.P., Deacon, L.J., 2005. Biodiversity of saprotrophic fungi in relation to their function: do fungi obey the rules? In: Bardgett, R.D., Usher, M.B., Hopkins, D.W. (Eds.), Biological diversity and function in soils. Cambridge University Press, Cambridge, pp. 189–215.Google Scholar
  31. Schimel, J.P., Gulledge, J., 1998. Microbial community structure and global trace gases. Glob Chang Biol 4, 745–758.CrossRefGoogle Scholar
  32. Schloss, P.D., Handelsman, J., 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71, 1501–1506.PubMedCrossRefGoogle Scholar
  33. Schoener, T.W., 1974. Resource partitioning in ecological communities. Science 185, 27–39.PubMedCrossRefGoogle Scholar
  34. Swift, M.J., Heal, O·W., Anderson, J.M., 1979. Decomposition in terrestrial ecosystems. Blackwell Scientific Publications, Oxford.Google Scholar
  35. Toljander, Y.K., Lindahl, B.D., Holmer, L., Högberg, N·O.S., 2006. Environmental fluctuations facilitate species co-existence and increase decomposition in communities of wood decay fungi. Oecologia 148, 625–631.PubMedCrossRefGoogle Scholar
  36. Torsvik, V., Øvreås, L., 2002. Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5, 240–245.PubMedCrossRefGoogle Scholar
  37. Treseder, K·K., 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164, 347–355.CrossRefGoogle Scholar
  38. Waksman, S.A., Nissen, W., 1931. Lignin as a nutrient for the cultivated mushroom, Agaricus campestris. Science 74, 271–2.PubMedCrossRefGoogle Scholar
  39. Waksman, S.A., Skinner, C.E., 1926. Microorganisms concerned in the decomposition of celluloses in the soil. Journal of Bacteriology 12, 57–84.PubMedGoogle Scholar
  40. Waksman, S.A., Tenney, F.G., Stevens, K.R., 1928. The role of microorganisms in the transformation of organic matter in forest soils. Ecology 9, 126–144.CrossRefGoogle Scholar
  41. Waldrop, M.P., Balser, T.C., Firestone, M.K., 2000. Linking microbial community composition to function in a tropical soil. Soil Biology & Biochemistry 32, 1837–1846.CrossRefGoogle Scholar
  42. Waldrop, M.P., Firestone, M.K., 2004. Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138, 275–284.PubMedCrossRefGoogle Scholar
  43. Waldrop, M.P., Zak, D.R., Blackwood, C·B., Curtis, C.D., Tilman, D., 2006. Resource availability controls fungal diversity across a plant diversity gradient. Ecology Letters 9, 1127–1135.PubMedCrossRefGoogle Scholar
  44. Wardle, D.A., 2006. The influence of biotic interactions on soil biodiversity. Ecology Letters 9, 870–886.PubMedCrossRefGoogle Scholar
  45. White, T.J., Bruns, T.D., Lee, S·B., Taylor, J.W., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: a guide to methods and application. Academic Press, Inc., New York, NY, pp. 315–322.Google Scholar
  46. Wolters, V., Silver, W.L., Bignell, D.E., Coleman, D.C., Lavelle, P., Van der Putten, W·H., De Ruiter, P., Rusek, J., Wall, D.H., Wardle, D.A., Brussaard, L., Dangerfield, J.M., Brown, V·K., Giller, K.E., Hooper, D.U., Sala, O., Tiedje, J., Van Veen, J.A., 2000. Effects of global changes on above- and belowground biodiversity in terrestrial ecosystems: implications for ecosystem functioning. Bioscience 50, 1089–1098.CrossRefGoogle Scholar
  47. Yin, B., Crowley, D., Sparovek, G., De Melo, W.J., Borneman, J., 2000. Bacterial functional redundancy along a soil reclamation gradient. Applied and Environmental Microbiology 66, 4361–4365.PubMedCrossRefGoogle Scholar
  48. Zak, J.C., Visser, S., 1996. An appraisal of soil fungal biodiversity: the crossroads between taxonomic and functional biodiversity. Biodiversity and Conservation 5, 169–183.CrossRefGoogle Scholar
  49. Zhou, J.Z., Xia, B·C., Treves, D.S., Wu, L.Y., Marsh, T.L., O’Neill, R.V., Palumbo, A.V., Tiedje, J.M., 2002. Spatial and resource factors influencing high microbial diversity in soil. Applied and Environmental Microbiology 68, 326–334.PubMedCrossRefGoogle Scholar
  50. Zogg, G.P., Zak, D.R., Ringelberg, D.B., MacDonald, N·W., Pregitzer, K·S., White, D.C., 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal 61, 475–481.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • China A. Hanson
    • 1
    Email author
  • Steven D. Allison
    • 1
  • Mark A. Bradford
    • 2
  • Matthew D. Wallenstein
    • 3
  • Kathleen K. Treseder
    • 1
  1. 1.Departments of Ecology and Evolutionary Biology and Earth System ScienceUniversity of CaliforniaIrvineUSA
  2. 2.Institute of EcologyUniversity of GeorgiaAthensUSA
  3. 3.Natural Resource Ecology LaboratoryColorado State UniversityFort CollinsUSA

Personalised recommendations