Advertisement

Microbial Ecology

, Volume 51, Issue 3, pp 302–314 | Cite as

Relationships Between Microbial Community Structure and Soil Processes Under Elevated Atmospheric Carbon Dioxide

  • David A. Lipson
  • Michelle Blair
  • Greg Barron-Gafford
  • Kathrine Grieve
  • Ramesh Murthy
Article

Abstract

There is little current understanding of the relationship between soil microbial community composition and soil processes rates, nor of the effect climate change and elevated CO2 will have on microbial communities and their functioning. Using the eastern cottonwood (Populus deltoides) plantation at the Biosphere 2 Laboratory, we studied the relationships between microbial community structure and process rates, and the effects of elevated atmospheric CO2 on microbial biomass, activity, and community structure. Soils were sampled from three treatments (400, 800, and 1200 ppm CO2), a variety of microbial biomass and activity parameters were measured, and the bacterial community was described by 16S rRNA libraries. Glucose substrate-induced respiration (SIR) was significantly higher in the 1200 ppm CO2 treatment. There were also a variety of complex, nonlinear responses to elevated CO2. There was no consistent effect of elevated CO2 on bacterial diversity; however, there was extensive variation in microbial community structure within the plantation. The southern ends of the 800 and 1200 ppm CO2 bays were dominated by β-Proteobacteria, and had higher fungal biomass, whereas the other areas contained more α-Proteobacteria and Acidobacteria. A number of soil process rates, including salicylate, glutamate, and glycine substrate-induced respiration and proteolysis, were significantly related to the relative abundance of the three most frequent bacterial taxa, and to fungal biomass. Overall, variation in microbial activity was better explained by microbial community composition than by CO2 treatment. However, the altered diversity and activity in the southern bays of the two high CO2 treatments could indicate an interaction between CO2 and light.

Keywords

Photosynthetically Active Radiation Clone Library Microbial Community Structure Microbial Community Composition Eastern Cottonwood 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We gratefully acknowledge Spring Strahm, Laura Dane, and Richard Wilson for logistical and laboratory assistance, and Dr. Barry Osmond for his skilled coordination of research efforts at B2L. The comments of two anonymous reviewers were very helpful in revising this manuscript. Financial support was provided by the Packard Foundation and the Office of the Executive Vice Provost, Columbia University (Dr. Michael Crow). We especially would like to thank Mr. Edward P. Bass for making this study possible.

References

  1. 1.
    Amann, RI, Ludwig, W, Schleifer, K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143–169PubMedGoogle Scholar
  2. 2.
    Anderson, JPE, Domsch, KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10: 215–221CrossRefGoogle Scholar
  3. 3.
    Ausebel, FM (Ed.) (1994) Current Protocols in Molecular Biology. Wiley, New YorkGoogle Scholar
  4. 4.
    Barron-Gafford, G, Martens, D, Grieve, K, Biel, K, Kudeyarov, V, McLain, JE, Lipson, D, Murthy, R (2005) Growth of eastern cottonwoods (Populus deltoides) in elevated CO2 stimulates stand-level respiration and rhizodeposition of carbohydrates, accelerates soil nutrient depletion, yet stimulates above and belowground biomass production. Global Change Biol 11: 1220–1233CrossRefGoogle Scholar
  5. 5.
    Colwell, RK (1997) EstimateS: Statistical estimation of species richness and shared species from samples. Version 5. User's Guide and application published at: http://viceroy.eeb.uconn.edu/estimates
  6. 6.
    Diaz, S, Grime, JP, Harris, J, McPherson, E (1993) Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364: 616–617CrossRefGoogle Scholar
  7. 7.
    Ebersberger, D, Werrnbter, N, Niklaus, PA, Kandeler, E (2004) Effects of long term CO2 enrichment on microbial community structure in calcareous grassland. Plant Soil 264: 313–323CrossRefGoogle Scholar
  8. 8.
    Engel, VC, Griffin, KL, Murthy, R, Patterson, L, Klimas, CA, Potosnak, MJ (2004) Growth CO2 modifies the transpiration response of Populus deltoides to drought and vapor pressure Q1 deficit. Tree Physiol 24: 1137–1145PubMedGoogle Scholar
  9. 9.
    Felsenstein, J (1989) PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5: 164–166Google Scholar
  10. 10.
    Field, CB, Lund, CP, Chiariello, NR, Mortimer, BE (1997) CO2 effects on the water budget of grassland microcosm communities. Global Change Biol 3: 197–206CrossRefGoogle Scholar
  11. 11.
    Grayston, SJ, Campbell, CD, Lutze, JL, Gifford, RM (1998) Impact of elevated CO2 on the metabolic diversity of microbial communities in N limited grass swards. Plant Soil 203: 289–300CrossRefGoogle Scholar
  12. 12.
    Griffiths, BS, Ritz, K, Ebblewhite, N, Paterson, E, Killham, K (1998) Ryegrass rhizosphere microbial community structure under elevated carbon dioxide concentrations, with observations on wheat rhizosphere. Soil Biol Biochem 30: 315–321CrossRefGoogle Scholar
  13. 13.
    Griffin, KL, Turnbull, M, Murthy, R, et al. (2002) Leaf respiration is differentially affected by leaf vs stand-level night-time warming. Global Change Biol 8: 479–485CrossRefGoogle Scholar
  14. 14.
    Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98Google Scholar
  15. 15.
    Horz, HP, Barbrook, A, Field, CB, Bohannan, BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. PNAS 101: 15136–15141CrossRefPubMedGoogle Scholar
  16. 16.
    Hugenholtz, P, Goebel, BM, Pace, NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765–4774PubMedGoogle Scholar
  17. 17.
    Hughes, JB, Hellmann, JJ, Ricketts, TH, Bohannan, BJ (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67: 4399–4406CrossRefPubMedGoogle Scholar
  18. 18.
    Hungate, BA, Holland, EA, Jackson, RB, Chapin, FS III, Mooney, HA, Field, HA (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388: 576–579CrossRefGoogle Scholar
  19. 19.
    Insam, H, Baath, E, Berreck, M, et al. (1999) Responses of the soil microbiota to elevated CO2 in an artificial tropical ecosystem. J Microbiol Methods 36: 45–54CrossRefPubMedGoogle Scholar
  20. 20.
    Körner, C (2000) Biosphere responses to CO2 enrichment. Ecol App 10: 1590–1619Google Scholar
  21. 21.
    Körner, C, Arnone, J III (1992) Responses to elevated carbon dioxide in artificial tropical ecosystems. Science 257: 1672–1675PubMedCrossRefGoogle Scholar
  22. 22.
    Körner, C, Diemer, M, Schäppi, B, Niklaus, P, Arnone, J III (1997) The responses of alpine grassland to four seasons of CO2 enrichment: a synthesis. Acta Oecologica 18: 165–175CrossRefGoogle Scholar
  23. 23.
    Lipson, DA, Schadt, CW, Schmidt, SK (2002) Changes in microbial community structure and function following snow melt in an alpine soil. Microb Ecol 43: 307–314CrossRefPubMedGoogle Scholar
  24. 24.
    Lipson, DA, Schmidt, SK, Monson, RK (1999) Links between microbial population dynamics and N availability in an alpine ecosystem. Ecology 80: 1623–1631CrossRefGoogle Scholar
  25. 25.
    Lipson, DA, Schmidt, SK (2004) Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl Environ Microb 70: 2867–2879CrossRefPubMedGoogle Scholar
  26. 26.
    Martin, AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microb 68: 3673–3682CrossRefGoogle Scholar
  27. 27.
    Mathieu-Daude, F, Welsh, J, Vogt, T, McClelland, M (1996) DNA rehybridization during PCR: the Cot effect and its consequences. Nucleic Acids Res 24: 2080–2086CrossRefPubMedGoogle Scholar
  28. 28.
    Mayr, C, Miller, M, Insam, H (1999) Elevated CO2 alters community level physiological profiles and enzyme activities in alpine grassland. J Microbiol Methods 36: 35–43CrossRefPubMedGoogle Scholar
  29. 29.
    Miller, DN, Bryant, JE, Madsen, EL, Ghiorse, WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microb 65: 4714–4715Google Scholar
  30. 30.
    Mitchell, EAD, Gilbert, D, Buttler, A, Amblard, C, Grosvernier, P, Gobalt, JM (2003) Structure of microbial communities in Sphagnum peatlands and effect of atmospheric carbon dioxide enrichment. Microb Ecol 46: 187–199CrossRefPubMedGoogle Scholar
  31. 31.
    Montealegre, CM, van Kessel, C, Russele, MP, Sadowsky, MJ (2002) Changes in microbial activity and composition in a pasture ecosystem exposed to elevated atmospheric carbon dioxide. Plant Soil 243: 197–207CrossRefGoogle Scholar
  32. 32.
    Murthy, R, Griffin, KL, Zarnoch, SJ, et al. (2003) Response of carbon dioxide efflux from a 550 m3 soil bed to a range of soil temperatures. Forest Ecol Management 178: 311–327Google Scholar
  33. 33.
    Murthy, R, Barron-Gafford, G, Dougherty, PM, et al. (2005) Increased leaf area dominates carbon flux response to elevated CO2 in stands of Populus deltoides (Bartr.) with higher fidelity in scaling leaf-stand processes under soil moisture stress. Global Change Biol 11: 716–773CrossRefGoogle Scholar
  34. 34.
    Osmond, B, Ananyevw, G, Berry, J, et al. (2004) Changing the way we think about global change research: scaling up in experimental ecosystem science. Global Change Biol 10: 393–407CrossRefGoogle Scholar
  35. 35.
    O’Neill, EG (1994) Response of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165: 55–65CrossRefGoogle Scholar
  36. 36.
    Pace, NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740CrossRefPubMedGoogle Scholar
  37. 37.
    Phillips, RL, Zak, DR, Holmes, WE, White, DC (2002) Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 131: 236–244CrossRefGoogle Scholar
  38. 38.
    Prior, SA, Torbert, HA, Runion, GB, et al. (1997) Free air carbon dioxide enrichment of wheat: soil carbon and nitrogen dynamics. J Environ Qual 26: 1161–1166Google Scholar
  39. 39.
    Randlett, DL, Zak, DR, Pregitzer, KS, Curtis, PS (1996) Elevated atmospheric carbon dioxide and leaf litter chemistry: influences on microbial respiration and net nitrogen mineralization. Soil Sci Soc Am J 60: 1571–1577CrossRefGoogle Scholar
  40. 40.
    Rillig, MC, Scow, KM, Klironomos, JN, Allen, MF (1997) Microbial carbon substrate utilization in the rhizosphere of Gutierrezia sarothrae grown in elevated atmospheric carbon dioxide. Soil Biol Biochem 29: 1387–1394CrossRefGoogle Scholar
  41. 41.
    Sait, M, Hugenholtz, P, Janssen, PH (2004) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4: 654–666CrossRefGoogle Scholar
  42. 42.
    Schmidt, SK (1992) A substrate-induced growth-response (SIGR) method for estimating the biomass of microbial functional groups in soil and aquatic systems. FEMS Microbiol Ecol 101: 197–206CrossRefGoogle Scholar
  43. 43.
    Schortemeyer, M, Hartwig, UA, Hendrey, GR, Sadowsky, MJ (1996) Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE). Soil Biol Biochem 28: 1717–1724CrossRefGoogle Scholar
  44. 44.
    Thompson, JD, Higgins, DG, Gibson, TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680PubMedCrossRefGoogle Scholar
  45. 45.
    Torbert, HA, Johnson, HB (2001) Soil of the intensive agriculture biome of Biosphere2. J Soil Water Conserv 56: 4–11Google Scholar
  46. 46.
    Torsvik, V, Øvreås, L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5: 240–245CrossRefPubMedGoogle Scholar
  47. 47.
    Tsai, YL, Olson, B (1992) Rapid method for separation of bacterial DNA from humic substances in sediments for polymerase chain reaction. Appl Environ Microbiol 58: 2292–2295PubMedGoogle Scholar
  48. 48.
    Van Ginkel, JH, Gorissen, A, Van Veen, JA (1996) Long term decomposition of grass roots as affected by elevated atmospheric carbon dioxide. J Environ Qual 25: 1122–1128CrossRefGoogle Scholar
  49. 49.
    Van Ginkel, JH, Gorissen, A, Polci, D (2000) Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition. Soil Biol Biochem 32: 49–456CrossRefGoogle Scholar
  50. 50.
    Williams, MA, Rice, CW, Owensby, CE (2000) Carbon dynamics and microbial activity in tallgrass prairie exposed to elevated CO2 for 8 years. Plant Soil 227: 127–137CrossRefGoogle Scholar
  51. 51.
    Zabel, B, Hawes, P, Hewitt, S, Marino, BDV (1999) Construction and engineering of a created environment: overview of the Biosphere 2 closed system. Ecol Eng 13: 43–63CrossRefGoogle Scholar
  52. 52.
    Zak, DR, Pregitzer, KS, Curtis, PS, Teeri, JA, Fogel, R, Randlett, DL (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles in forested ecosystems. Plant Soil 151: 105–117CrossRefGoogle Scholar
  53. 53.
    Zak, DR, Pregitzer, KS, Curtis, PS, Holmes, WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10: 47–59Google Scholar
  54. 54.
    Zak, DR, Pregitzer, KS, King, JS, Holmes, WE (2000) Elevated atmospheric CO2, fine roots and the response of soil micro-organisms: a review and hypothesis. New Phytol 147: 201–222CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • David A. Lipson
    • 1
  • Michelle Blair
    • 1
  • Greg Barron-Gafford
    • 2
  • Kathrine Grieve
    • 2
  • Ramesh Murthy
    • 2
  1. 1.Department of BiologySan Diego State UniversitySan DiegoUSA
  2. 2.Biosphere2 LaboratoryOracleUSA

Personalised recommendations