Skip to main content
Log in

Microbial community shifts influence patterns in tropical forest nitrogen fixation

  • Ecosystem ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The role of biodiversity in ecosystem function receives substantial attention, yet despite the diversity and functional relevance of microorganisms, relationships between microbial community structure and ecosystem processes remain largely unknown. We used tropical rain forest fertilization plots to directly compare the relative abundance, composition and diversity of free-living nitrogen (N)-fixer communities to in situ leaf litter N fixation rates. N fixation rates varied greatly within the landscape, and ‘hotspots’ of high N fixation activity were observed in both control and phosphorus (P)-fertilized plots. Compared with zones of average activity, the N fixation ‘hotspots’ in unfertilized plots were characterized by marked differences in N-fixer community composition and had substantially higher overall diversity. P additions increased the efficiency of N-fixer communities, resulting in elevated rates of fixation per nifH gene. Furthermore, P fertilization increased N fixation rates and N-fixer abundance, eliminated a highly novel group of N-fixers, and increased N-fixer diversity. Yet the relationships between diversity and function were not simple, and coupling rate measurements to indicators of community structure revealed a biological dynamism not apparent from process measurements alone. Taken together, these data suggest that the rain forest litter layer maintains high N fixation rates and unique N-fixing organisms and that, as observed in plant community ecology, structural shifts in N-fixing communities may partially explain significant differences in system-scale N fixation rates.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 110:135–145

    Article  Google Scholar 

  • Alexander V, Schell DM (1973) Seasonal and spatial variation of nitrogen fixation in the Barrow, Alaska. Tundra Arc Alp Res 5:77–88

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang ZH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415

    Article  CAS  Google Scholar 

  • Belnap J (1996) Soil surface disturbance in cold deserts: effects on nitrogenase activity in cyanobacterial-lichen soil crusts. Biol Fert Soils 23:362–367

    Article  CAS  Google Scholar 

  • Benner JW, Vitousek PM (2007) Development of a diverse epiphyte community in response to phosphorus fertilization. Ecol Lett 10:628–636

    Article  PubMed  Google Scholar 

  • Bern CR, Townsend AR, Farmer GL (2005) Unexpected dominance of parent-material strontium in a tropical forest on highly weathered soils. Ecology 86:626–632

    Article  Google Scholar 

  • Berrange JP, Thorpe RS (1988) The geology, geochemistry and emplacement of the cretaceous tertiary ophiolitic Nicoya complex of the Osa Peninsula, southern Costa Rica. Tectonophysics 147:193–199

    Article  CAS  Google Scholar 

  • Carney KM, Matson PA, Bohannan BJM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land use types. Ecol Lett 7:684–694

    Article  Google Scholar 

  • Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414

    Article  Google Scholar 

  • Christensen S, Simkins S, Tiedje JM (1990) Spatial variation in denitrification. Soil Sci Soc Am J 54:1608–1613

    Article  CAS  Google Scholar 

  • Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 104:10316–10321

    Article  Google Scholar 

  • Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, von Fischer JC, Elseroad A, Wasson M (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochem Cycles 13:545–623

    Article  Google Scholar 

  • Cleveland CC, Reed SC, Townsend AR (2006) Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87:492–503

    Article  PubMed  Google Scholar 

  • Compton JE, Watrud LS, Porteous LA, DeGrood S (2004) Response of soil microbial biomass a and community composition to chronic nitrogen additions at Harvard forest. For Ecol Manag 196:143–158

    Article  Google Scholar 

  • Davidson EA, Ishida FY, Nepstad DC (2004) Effects of an experimental drought on soil e emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical f forest. Global Change Biol 10:718–730

    Article  Google Scholar 

  • Eisele KA, Schimel DS, Kapustka LA, Parton WJ (1989) Effects of available phosphorus and nitrogen-phosphorus ratios on non-symbiotic dinitrogen fixation in tallgrass prairie soils. Oecologia 79:471–474

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  • Gehring C, Vlek PLG, de Souza LAG, Denich M (2005) Biological nitrogen fixation in secondary regrowth and mature rain forests of central Amazonia. Agric Ecosyst Environ 111:237–252

    Article  CAS  Google Scholar 

  • Groffman PM, Butterbach-Bahl K, Fulweiler RW, Gold AJ, Morse JL, Stander EK, Tauge C, Tonitto C, Vidon P (2009) Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93:49–77

    Article  CAS  Google Scholar 

  • Gulledge J, Doyle AP, Schimel JP (1997) Different NH4 +-inhibition patterns of soil CH4 consumption: a result of distinct CH4-oxidzer populations across sites? Soil Biol Biochem 29:13–21

    Article  CAS  Google Scholar 

  • Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Phys 43:1185–1207

    Article  CAS  Google Scholar 

  • Harry M, Gambier B, Garnier-Sillam E (2000) Soil conservation for DNA preservation for bacterial molecular studies. Eur J Soil Biol 36:51–55

    Article  CAS  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • Hicks WT, Harmon ME, Griffiths RP (2003) Abiotic controls on nitrogen fixation and respiration in selected woody debris from the Pacific Northwest, USA. Ecoscience 10:66–73

    Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Horner-Devine MC, Martiny AC (2008) News about nitrogen. Science 320:757–758

    Article  CAS  PubMed  Google Scholar 

  • Howarth RW, Marino R, Cole JJ (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol Oceanogr 33:688–701

    Article  CAS  Google Scholar 

  • Hsu SF, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3:124–136

    Article  CAS  PubMed  Google Scholar 

  • Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kabir S, Rajendran T, Amemiya T, Itoh K (2003) Quantitative measurement of fungal DNA extracted by three different methods using real-time polymerase chain reaction. J Biosci Bioeng 96:337–343

    CAS  PubMed  Google Scholar 

  • Kappelle M, Castro M, Acevedo H, Gonzalez L, Monge H (2002) Ecosystems of the Osa Conservation Area (ACOSA). Instituto Nacional Biodiversidad (INBio), Costa Rica

  • Lewis LA, Lewis PO (2005) Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Syst Biol 54:936–947

    Article  PubMed  Google Scholar 

  • Ley RE, D’Antonio CM (1998) Exotic grass invasion alters potential rates of N fixation in Hawaiian woodlands. Oecologia 113:179–187

    Article  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 1:8228–8235

    Article  Google Scholar 

  • Martiny JBH, Bohannan B, Brown J, Colwell R, Fuhrman J, Green J, Horner-Devine MC, Kane M, Krumins J, Kuske C, Morin P, Naeem S, Ovreas L, Reysenbach AL, Smith V, Staley J (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  PubMed  Google Scholar 

  • McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312

    Article  CAS  Google Scholar 

  • Moré 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  Google Scholar 

  • Moseman SM, Zhang R, Quan PY, Levin LA (2009) Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biol Invasions 11:225–239

    Article  Google Scholar 

  • Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122

    Article  PubMed  Google Scholar 

  • Park JW, Crowley DE (2005) Normalization of soil DNA extraction for accurate quantification of real-time PCR and of target genes by DGGE. Biotechniques 38:579–586

    Article  CAS  PubMed  Google Scholar 

  • Parkin TB (1987) Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 51:1194–1199

    Article  CAS  Google Scholar 

  • Perez SE, Perez CA, Carmona MR, Farina JM, Armesto JJ (2008) Effects of labile phosphorus and carbon on non-symbiotic N-2 fixation in logged and unlogged evergreen forests in Chiloe Island, Chile. Rev Chil Hist Nat 81:267–278

    Article  Google Scholar 

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

    Article  CAS  PubMed  Google Scholar 

  • Reed HE, Martiny JBH (2007) Testing the functional significance of microbial composition in natural communities. FEMS Microbiol Ecol 62:161–170

    Article  CAS  PubMed  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2007a) Controls over leaf litter and soil nitrogen fixation in two lowland tropical rain forests. Biotropica 39:585–592

    Article  Google Scholar 

  • Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007b) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2008) Tree species control rates of free-living nitrogen fixation in a tropical rain forest. Ecology 89:2924–2934

    Article  PubMed  Google Scholar 

  • Roskoski JP (1980) Nitrogen fixation in hardwood forests of the northeastern United States. Plant Soil 54:33–44

    Article  CAS  Google Scholar 

  • Shaffer BT, Widmer F, Porteous LA, Seidler RJ (2000) Temporal and spatial distribution of the nifH gene of N2fixing bacterial in forests and cleacuts in western Oregon. Microb Ecol 39:12–21

    Article  CAS  PubMed  Google Scholar 

  • Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416

    Article  Google Scholar 

  • Sprent JI, Sprent P (1990) Nitrogen fixing organisms. Chapman and Hall, London

    Google Scholar 

  • Stamatakis A (2006) RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Swofford DL (2001) Phylogenetic analysis using parsimony, 4th edn. Sinauer, Sunderland

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Townsend AR, Martinelli LA, Howarth RW (2009) The global nitrogen cycle, biodiversity, and human health. In: Sala OE, Meyerson LA (eds) Biodiversity change and human health. Island Press, Washington, DC, pp 159–179

    Google Scholar 

  • Vitousek P, Hobbie S (2000) Heterotrophic nitrogen fixation in decomposing litter: patterns, mechanisms, and models. Ecology 75:418–429

    Article  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  • Waldrop MP, Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol 52:470–479

    Article  CAS  PubMed  Google Scholar 

  • Wallenstein MD, Vilgalys RJ (2005) Quantitative analyses of nitrogen cycling genes in soils. Pedobiologia 49:665–672

    Article  CAS  Google Scholar 

  • Widmer F, Shaffer BT, Porteous LA, Seidler RJ (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas Fir forest site in the oregon cascade mountain range. Appl Environ Microbiol 65:374–380

    CAS  PubMed  Google Scholar 

  • Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske C (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the colorado plateau and Chihuahuan desert. Appl Environ Microbiol 70:973–983

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work benefited enormously from the assistance of S. Schmidt, E. Costello, R. Kysela, M. Robeson, S. Sattin, J. Metcalf, N. Fierer, A. Martin and R. Jones. We are grateful to W. Bowman, J. Neff, and T. Seastedt for discussions that shaped this research and to two anonymous reviewers for their insightful suggestions. We thank A. Michaud and A. Vega for help with sample collection, J. Feis, N. Ascarrunz and W. Wieder for laboratory assistance, and H. and M. Michaud, F. Campos and the Organization for Tropical Studies (OTS) and the Ministerio de Ambiente y Energia (MINAE) in Costa Rica, for logistical support. Support was provided by National Science Foundation grants DEB-0136957 to C.C. and A.T., DEB-00852916 to C.C., D.N. and A.T., DEB-0710404 to A.T. and S.R., and a graduate research fellowship to S.R., as well as grants to A.T. and C.C. from the Andrew W. Mellon Foundation. These experiments all conformed with the current laws of the country in which they were performed and the authors have no conflicts of interests. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sasha C. Reed.

Additional information

Communicated by Michael Madritch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (227 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reed, S.C., Townsend, A.R., Cleveland, C.C. et al. Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164, 521–531 (2010). https://doi.org/10.1007/s00442-010-1649-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1649-6

Keywords

Navigation