Skip to main content

Advertisement

SpringerLink
Log in

Elevated Atmospheric CO2 Impacts Abundance and Diversity of Nitrogen Cycling Functional Genes in Soil

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The concentration of CO2 in the Earth's atmosphere has increased over the last century. Although this increase is unlikely to have direct effects on soil microbial communities, increased atmospheric CO2 may impact soil ecosystems indirectly through plant responses. This study tested the hypothesis that exposure of plants to elevated CO2 would impact soil microorganisms responsible for key nitrogen cycling processes, specifically denitrification and nitrification. We grew trembling aspen (Populus tremuloides) trees in outdoor chambers under ambient (360 ppm) or elevated (720 ppm) levels of CO2 for 5 years and analyzed the microbial communities in the soils below the trees using quantitative polymerase chain reaction and clone library sequencing targeting the nitrite reductase (nirK) and ammonia monooxygenase (amoA) genes. We observed a more than twofold increase in copy numbers of nirK and a decrease in nirK diversity with CO2 enrichment, with an increased predominance of Bradyrhizobia-like nirK sequences. We suggest that this dramatic increase in nirK-containing bacteria may have contributed to the significant loss of soil N in the CO2-treated chambers. Elevated CO2 also resulted in a significant decrease in copy numbers of bacterial amoA, but no change in archaeal amoA copy numbers. The decrease in abundance of bacterial amoA was likely a result of the loss of soil N in the CO2-treated chambers, while the lack of response for archaeal amoA supports the hypothesis that physiological differences in these two groups of ammonia oxidizers may enable them to occupy distinct ecological niches and respond differently to environmental change.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    PubMed  CAS  Google Scholar 

  2. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57

    Article  CAS  Google Scholar 

  3. Ball AS, Drake BG (1997) Short-term decomposition of litter produced by plants grown in ambient and elevated atmospheric CO 2 concentrations. Global Change Biol 3:29

    Article  Google Scholar 

  4. Blagodatskaya E, Blagodatsky S, Dorodnikov M, Kuzyakov Y (2010) Elevated atmospheric CO2 increases microbial growth rates in soil: results of three CO2 enrichment experiments. Global Change Biol 16:836

    Article  Google Scholar 

  5. Braker G, Ayala-del-Rio HL, Devol AH, Fesefeldt A, Tiedje JM (2001) Community structure of denitrifiers, Bacteria, and Archaea along redox gradients in Pacific Northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl Environ Microbiol 67:1893

    Article  PubMed  CAS  Google Scholar 

  6. Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769

    PubMed  CAS  Google Scholar 

  7. Cardon ZG, Hungate BA, Cambardella CA, Chapin FS III, Field CB, Holland EA, Mooney HA (2001) Contrasting effects of elevated CO2 on old and new soil carbon pools. Soil Biol Biochem 33:365

    Article  CAS  Google Scholar 

  8. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci USA 104:4990

    Article  PubMed  CAS  Google Scholar 

  9. Ceulemans R, Mousseau M (1994) Effects of elevated atmospheric CO2 on woody plants. New Phytol 127:425

    Article  Google Scholar 

  10. Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759

    Article  PubMed  CAS  Google Scholar 

  11. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265

    Google Scholar 

  12. Chow S, Rodgers P (2005) Constructing area-proportional Venn and Euler diagrams with three circles. Euler Diagrams Workshop, Paris

    Google Scholar 

  13. Cotrufo MF, Ineson P (1996) Elevated CO 2 reduces field decomposition rates of Betula pendula (Roth.) leaf litter. Oecologia 106:525

    Article  Google Scholar 

  14. Curtis PS, Zak DR, Pregitzer KS, Lussenhop J, Teeri JA (1996) Linking above- and belowground responses to rising CO 2 in northern deciduous forest species. In: Koch GW, Mooney HA (eds) Carbon dioxide and terrestrial ecosystems. Academic, New York, pp 41–52

    Chapter  Google Scholar 

  15. Curtis PS, Teeri JA (1992) Seasonal responses of leaf gas exchange to elevated carbon dioxide in Populus grandidentata. Can J Forest Res 22:1320

    Article  CAS  Google Scholar 

  16. De Angelis P, Chigwerewe KS, Scarascia Mugnozza GE (2000) Litter quality and decomposition in a CO2-enriched Mediterranean forest ecosystem. Plant Soil 224:31

    Article  Google Scholar 

  17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194

    Article  PubMed  CAS  Google Scholar 

  18. Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121

    Article  PubMed  CAS  Google Scholar 

  19. Falk S, Liu B, Braker G (2010) Isolation, genetic and functional characterization of novel soil nirK-type denitrifiers. Syst Appl Microbiol 33:337

    Article  PubMed  CAS  Google Scholar 

  20. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing Archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683

    Article  PubMed  CAS  Google Scholar 

  21. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biology 4:520

    Article  CAS  Google Scholar 

  22. He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing Archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364

    Article  PubMed  CAS  Google Scholar 

  23. He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, Van Nostrand JD, Hobbie SE, Reich PB, Zhou J (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13:564

    Article  PubMed  Google Scholar 

  24. Herndl GJ, Reinthaler T, Teira E, Van Aken H, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303

    Article  PubMed  CAS  Google Scholar 

  25. Holmes WE, Zak DR, Pregitzer KS, King JS (2003) Soil nitrogen transformations under Populus tremuloides, Betula papyrifera and Acer saccharum following 3 years exposure to elevated CO2 and O3. Global Change Biol 9:1743

    Article  Google Scholar 

  26. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge

    Google Scholar 

  27. Hu S, Chapin FS, Firestone MK, Field CB, Chiariello NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:188

    Article  PubMed  CAS  Google Scholar 

  28. Hungate BA, Holland EA, Jackson RB, Chapin FS III, Mooney HA, Field CB (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388:576

    Article  CAS  Google Scholar 

  29. Insam H, Bååth E, Berreck M, Frostegård Å, Gerzabek MH, Kraft A, Schinner F, Schweiger P, Tschuggnall G (1999) Responses of the soil microbiota to elevated CO2 in an artificial tropical ecosystem. J Microbiol Methods 36:45

    Article  PubMed  CAS  Google Scholar 

  30. Janus LR, Angeloni NL, McCormack J, Rier ST, Tuchman NC, Kelly JJ (2005) Elevated atmospheric CO 2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots. Microb Ecol 50:102

    Article  PubMed  Google Scholar 

  31. Johnson DW, Hungate BA, Dijkstra P, Hymus G, Drake B (2001) Effects of elevated carbon dioxide on soils in a Florida scrub oak ecosystem. J Environ Qual 30:501

    Article  PubMed  CAS  Google Scholar 

  32. Kandeler E, Tscherko D, Bardgett R, Hobbs P, Kampichler C, Jones T (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem. Plant Soil 202:251

    Article  CAS  Google Scholar 

  33. Kelly JJ, Policht K, Grancharova T, Hundal LS (2011) Distinct responses in ammonia-oxidizing Archaea and Bacteria after addition of biosolids to an agricultural soil. Appl Environ Microbiol 77:6551

    Article  PubMed  CAS  Google Scholar 

  34. Koizumi H, Nakadai T, Usami Y, Satoh M, Shiyomi M, Oikawa T (1991) Effect of carbon dioxide concentration on microbial respiration in soil. Ecol Res 6:227

    Article  Google Scholar 

  35. Könneke M, Bernhard AE, De la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543

    Article  PubMed  Google Scholar 

  36. Kowalchuk GA, Stienstra AW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99

    Article  PubMed  CAS  Google Scholar 

  37. Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiol Ecol 31:207

    Article  PubMed  CAS  Google Scholar 

  38. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806

    Article  PubMed  CAS  Google Scholar 

  39. Lesaulnier C, Papamichail D, McCorkle S, Ollivier B, Skiena S, Taghavi S, Zak D, Van Der Lelie D (2008) Elevated atmospheric CO2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926

    Article  PubMed  CAS  Google Scholar 

  40. Lindroth RL, Kinney KK, Platz CL (1993) Responses of diciduous trees to elevated atmospheric CO2: productivity, phytochemistry, and insect performance. Ecology 74:763

    Article  CAS  Google Scholar 

  41. Lipson DA, Wilson RF, Oechel WC (2005) Effects of elevated atmospheric CO2 on soil microbial biomass, activity, and diversity in a chaparral ecosystem. Appl Environ Microbiol 71:8573

    Article  PubMed  CAS  Google Scholar 

  42. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Ann Rev Plant Biol 55:591

    Article  CAS  Google Scholar 

  43. Mikan CJ, Zak DR, Kubiske ME, Pregitzer KS (2000) Combined effects of atmospheric CO 2 and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms. Oecologia 124:432

    Article  Google Scholar 

  44. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162

    Article  PubMed  CAS  Google Scholar 

  45. Mintie AT, Heichen RS, Cromack K Jr, Myrold DD, Bottomley PJ (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Appl Environ Microbiol 69:3129

    Article  PubMed  CAS  Google Scholar 

  46. Mußmann M, Brito I, Pitcher A, Damsté JSS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Müller A, Daims H (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci USA 108:16771

    Article  PubMed  Google Scholar 

  47. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing Archaea and Bacteria. Environ Microbiol 10:2966

    Article  PubMed  CAS  Google Scholar 

  48. Niklaus PA, Kandeler E, Leadley PW, Schmid B, Tscherko D, Körner C (2001) A link between plant diversity, elevated CO2 and soil nitrate. Oecologia 127:540

    Article  Google Scholar 

  49. Norby RJ, O'neill EG, Hood WG, Luxmoore RJ (1987) Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment. Tree Physiol 3:203

    Article  PubMed  Google Scholar 

  50. Ouverney CC, Fuhrman JA (2000) Marine planktonic Archaea take up amino acids. Appl Environ Microbiol 66:4829

    Article  PubMed  CAS  Google Scholar 

  51. Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, Vogel CS (1995) Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytol 129:579

    Article  Google Scholar 

  52. Prentice IC, Farquhar GD, Fasham MJR, Goulden ML, Heimann M, Jaramillo VJ, Kheshgi HS, Le Quéré C, Scholes RJ, Wallace DWR (2001) The carbon cycle and atmospheric carbon dioxide. In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (eds) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge, pp 183–237

    Google Scholar 

  53. Priemé A, Braker G, Tiedje JM (2002) Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils. Appl Environ Microbiol 68:1893

    Article  PubMed  Google Scholar 

  54. Rice CW, Garcia FO, Hampton CO, Owensby CE (1994) Soil microbial response in tallgrass prairie to elevated CO2. Plant Soil 165:67

    Article  CAS  Google Scholar 

  55. Rich JJ, Heichen RS, Bottomley PJ, Cromack K Jr, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974

    Article  PubMed  CAS  Google Scholar 

  56. Rosch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68:3818

    Article  PubMed  CAS  Google Scholar 

  57. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704

    PubMed  CAS  Google Scholar 

  58. Sadowsky M, Schortemeyer M (1997) Soil microbial responses to increased concentrations of atmospheric CO2. Global Change Biol 3:217

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  60. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537

    Article  PubMed  CAS  Google Scholar 

  61. Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Hoflich G, Hartmann A (1997) Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038

    PubMed  CAS  Google Scholar 

  62. Schmidt TL, Spencer JS Jr, Bertsch R (1997) Michigans forests 1993: an analysis. Resource Bulletin NC-179. USDA Forest Service, North Central Forest Experiment Station, St. Paul

    Google Scholar 

  63. Shen J, Zhang L, Zhu Y, Zhang J, He J (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing Archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601

    Article  PubMed  CAS  Google Scholar 

  64. Strain BR, Bazzaz FA (1983) Terrestrial plant communities. In: Lemon EH (ed) The response of plants to rising levels of atmospheric carbon dioxide. American Association for the Advancement of Science, Washington, pp 117–222

    Google Scholar 

  65. Strnad H, Ridl J, Paces J, Kolar M, Vlcek C, Paces V (2011) Complete genome sequence of the haloaromatic acid-degrading bacterium Achromobacter xylosoxidans A8. J Bacteriol 193:791

    Article  PubMed  CAS  Google Scholar 

  66. Sullivan JT, Eardly BD, van Berkum P, Ronson CW (1996) Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol 62:2818

    PubMed  CAS  Google Scholar 

  67. Tan Z, Hurek T, Vinuesa P, Muller P, Ladha JK, Reinhold-Hurek B (2001) Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Appl Environ Microbiol 67:3655

    Article  PubMed  CAS  Google Scholar 

  68. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing Archaea and Bacteria in soil microcosms. Environ Microbiol 10:1357

    Article  PubMed  CAS  Google Scholar 

  69. 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 32:449

    Article  Google Scholar 

  70. Wetzel RG, Grace JB (1983) Atmospheric CO2 enrichment effects on aquatic plants. In: Lemon EH (ed) The response of plants to rising levels of atmospheric carbon dioxide. American Association for the Advancement of Science, Washington, pp 223–280

    Google Scholar 

  71. Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL (1993) Elevated atmospheric CO 2 and feedback between carbon and nitrogen cycles. Plant Soil 151:105

    Article  CAS  Google Scholar 

  72. Zak DR, Pregitzer KS (1990) Spatial and temporal variability of nitrogen cycling in Northern Lower Michigan. For Sci 36:367

    Google Scholar 

Download references

Acknowledgements

Soils analyzed in this project were collected at the Elevated CO2 Research Facility of the University of Michigan Biological Station, where infrastructural support was provided by the US DOE National Institute of Global Environmental Change (NIGEC). This research was supported, in part, by grants awarded to N.C.T. from the National Science Foundation (DEB-9903888 and DEB-0108847) and by a supplement to grant DEB-0108847 awarded to N.C.T. and J.J.K. from the National Science Foundation. T.W. was supported by the Loyola University Chicago NSF REU Program in Bioinformatics (DBI 0552888). E.P. was supported by a Loyola University Chicago Provost Fellowship. The authors thank Kesha Baxi and Sara Idleman for their contributions to clone library preparation.

Author information

Authors and Affiliations

  1. Department of Biology, Loyola University Chicago, 1032 West Sheridan Road, Chicago, IL, 60660, USA

    John J. Kelly, Emily Peterson, Jonathan Winkelman & Nancy C. Tuchman

  2. Department of Biology, Carleton College, Northfield, MN, 55057, USA

    Teagan J. Walter

  3. Department of Biological and Allied Health Sciences, Bloomsburg University, Bloomsburg, PA, 17815, USA

    Steven T. Rier

Authors
  1. John J. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan Winkelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Teagan J. Walter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steven T. Rier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nancy C. Tuchman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John J. Kelly.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kelly, J.J., Peterson, E., Winkelman, J. et al. Elevated Atmospheric CO2 Impacts Abundance and Diversity of Nitrogen Cycling Functional Genes in Soil. Microb Ecol 65, 394–404 (2013). https://doi.org/10.1007/s00248-012-0122-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0122-y

Keywords

Search

Navigation