Advertisement

Oecologia

, Volume 154, Issue 2, pp 349–359 | Cite as

Microbial responses to nitrogen addition in three contrasting grassland ecosystems

  • Lydia H. ZeglinEmail author
  • Martina Stursova
  • Robert L. Sinsabaugh
  • Scott L. Collins
Ecosystem Ecology

Abstract

The effects of global N enrichment on soil processes in grassland ecosystems have received relatively little study. We assessed microbial community response to experimental increases in N availability by measuring extracellular enzyme activity (EEA) in soils from three grasslands with contrasting edaphic and climatic characteristics: a semiarid grassland at the Sevilleta National Wildlife Refuge, New Mexico, USA (SEV), and mesic grasslands at Konza Prairie, Kansas, USA (KNZ) and Ukulinga Research Farm, KwaZulu-Natal, South Africa (SAF). We hypothesized that, with N enrichment, soil microbial communities would increase C and P acquisition activity, decrease N acquisition activity, and reduce oxidative enzyme production (leading to recalcitrant soil organic matter [SOM] accumulation), and that the magnitude of response would decrease with soil age (due to higher stabilization of enzyme pools and P limitation of response). Cellulolytic activities followed the pattern predicted, increasing 35–52% in the youngest soil (SEV), 10–14% in the intermediate soil (KNZ) and remaining constant in the oldest soil (SAF). The magnitude of phosphatase response did not vary among sites. N acquisition activity response was driven by the enzyme closest to its pH optimum in each soil: i.e., leucine aminopeptidase in alkaline soil, β-N-acetylglucosaminidase in acidic soil. Oxidative enzyme activity varied widely across ecosystems, but did not decrease with N amendment at any site. Likewise, SOM and %C pools did not respond to N enrichment. Between-site variation in both soil properties and EEA exceeded any treatment response, and a large portion of EEA variability (leucine aminopeptidase and oxidative enzymes), 68% as shown by principal components analysis, was strongly related to soil pH (r = 0.91, P < 0.001). In these grassland ecosystems, soil microbial responses appear constrained by a molecular-scale (pH) edaphic factor, making potential breakdown rates of SOM resistant to N enrichment.

Keywords

Extracellular enzyme activity Soil carbon 

Notes

Acknowledgements

Funding for this work was provided by the National Science Foundation, the Sevilleta Long-Term Ecological Research (LTER) Program, the Konza Prairie LTER Program, the Ukulinga Research Farm (South Africa) and the University of KwaZulu-Natal (South Africa). Support of data collection and analysis was provided by Cliff Dahm, Chris Lauber, Marcy Gallo, John Blair, Alan Knapp, Melinda Smith, Rich Fynn, Chelsea Crenshaw, Nathan Daves-Brody, Kris Mossberg, Kylea Odenbach and John Craig. This article was improved by comments from Dr. Jason Kaye and three anonymous reviewers. The experiments described herein comply with the current laws of the countries in which they were performed.

References

  1. Aber J, McDowell W, Nadelhoffer K, Magill A, Bernston G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems: hypotheses revisited. BioScience 48:921–934CrossRefGoogle Scholar
  2. Aber JD, Goodale CL, Ollinger SV, Smith ML, Magill AH, Martin ME, Hallett RA, Stoddard JL (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? BioScience 53:375–389CrossRefGoogle Scholar
  3. Ajwa HA, Dell CJ, Rice CW (1999) Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization. Soil Biol Biochem 31:769–777CrossRefGoogle Scholar
  4. Allison SD, Gartner T, Holland K, Weintraub M, Sinsabaugh RL (2007) Soil enzymes: linking proteomics and ecological process. Manual of environmental microbiology. ASMGoogle Scholar
  5. Báez S, Fargione J, Moore DI, Collins SL, Gosz JR (2007) Atmospheric nitrogen deposition in the northern Chihuahuan Desert: temporal trends and potential consequences. J Arid Environ 68:640–651CrossRefGoogle Scholar
  6. Barrett JE, Burke IC (2000) Potential nitrogen immobilization in grassland soils across a soil organic matter gradient. Soil Biol Biochem 32:1707–1716CrossRefGoogle Scholar
  7. Barrett JE, Burke IC (2002) Nitrogen retention in semiarid ecosystems across a soil organic matter gradient. Ecol Appl 12:878–890CrossRefGoogle Scholar
  8. Blackwood CB, Waldrop MP, Zak DR, Sinsabaugh RL (2007) Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environ Microbiol 9:1306–1316Google Scholar
  9. Blair JM, Seastedt TR, Rice CW, Ramundo RA (1998) Terrestrial nutrient cycling in tallgrass prairie. In: Knapp AK, Briggs JM, Hartnett DC, Collins SC (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New York, 222–243Google Scholar
  10. Bond WJ, Woodward FI, Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytol 165:525–538PubMedCrossRefGoogle Scholar
  11. Buxbaum CAZ, Vanderbilt K (2007) Soil heterogeneity and the distribution of desert and steppe plant species across a desert–grassland ecotone. J Arid Environ 69:617–632CrossRefGoogle Scholar
  12. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  13. Clark FE (1977) Internal cycling of nitrogen in shortgrass prairie. Ecology 58:1322–1333CrossRefGoogle Scholar
  14. Corkidi L, Rowland DL, Johnson NC, Allen EB (2002) Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands. Plant Soil 240:299–310CrossRefGoogle Scholar
  15. Dijkstra FA, Hobbie SE, Knops JMH, Reich PB (2004) Nitrogen deposition and plant species interact to influence soil carbon stabiliztion. Ecol Lett 7:1192–1198CrossRefGoogle Scholar
  16. Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496CrossRefGoogle Scholar
  17. Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev Camb Philos Soc 63:433–462Google Scholar
  18. Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the community structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage 196:159–171CrossRefGoogle Scholar
  19. Fynn RWS, O’Connor TG (2005) Determinants of community organization of a south african mesic grassland. J Veg Sci 16:93–102CrossRefGoogle Scholar
  20. Gallo ME, Amonette R, Lauber CL, Sinsabaugh RL, Zak D (2004) Short-term changes in oxidative enzyme activity and microbial community structure in nitrogen-amended north temperate forest soils. Microb Ecol 48:218–229PubMedCrossRefGoogle Scholar
  21. Galy-Lacaux C, Ourabi HA, Lacaux JP, Gardrat E, Mphepya J, Pienaar K (2003) Dry and wet atmospheric nitrogen deposition in Africa. Geophys Res Abstr 5:09644Google Scholar
  22. Garcia FO, Rice CW (1994) Microbial biomass dynamics in tallgrass prairie. Soil Sci Soc Am J 58:816–823CrossRefGoogle Scholar
  23. Gosz JR, Moore DI, Shore GA, Grover HD, Rison W, Rison C (1995) Lightning estimates of precipitation location and quantity on the Sevilleta Lter, New-Mexico. Ecol Appl 5:1141–1150CrossRefGoogle Scholar
  24. Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb Ecol 47:104–113PubMedCrossRefGoogle Scholar
  25. Gundersen P, Emmett BA, Kjonass OJ, Koopmans CJ, Tietma A (1998) Impact of nitrogen cycling in forests: a synthesis of nitrex data. For Ecol Manage 101:37–55CrossRefGoogle Scholar
  26. Hammel KE (1997) Fungal degradation of lignin. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, pp 33–46Google Scholar
  27. Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob Change Biol 11:1808–1815CrossRefGoogle Scholar
  28. Higuchi T (1990) Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24:23–63CrossRefGoogle Scholar
  29. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  30. Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1985–1908Google Scholar
  31. Johnson D, Leake JR, Read DJ (2005) Liming and nitrogen fertilization affects phosphatase activities, microbial biomass and mycorrhizal colonisation in upland grassland. Plant Soil 271:157–164CrossRefGoogle Scholar
  32. Kaye J, Barrett J, Burke I (2002) Stable nitrogen and carbon pools in grassland soils of variable texture and carbon content. Ecosystems 5:461–471CrossRefGoogle Scholar
  33. Kennedy N, Brodie E, Connolly J, Clipson N (2004) Impact of lime, nitrogen and plant species on bacterial community structure in grassland microcosms. Environ Microbiol 6:1070–1080PubMedCrossRefGoogle Scholar
  34. Kieft TL, White CS, Loftin SR, Aguilar R, Craig JA, Skaar DA (1998) Temporal dynamics in soil carbon and nitrogen resources at a grassland-shrubland ecotone. Ecology 79:671–683Google Scholar
  35. Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–484PubMedCrossRefGoogle Scholar
  36. Knapp AK, Briggs JM, Blair JM, Turner CL (1998) Patterns and controls of aboveground net primary production in tallgrass prairie. In: Knapp AK, Briggs JM, Hartnett DC, Collins SC (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New York, pp 193–221Google Scholar
  37. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257CrossRefGoogle Scholar
  38. Lajtha K, Schlesinger WH (1988) The biogeochemistry of phosphorus cycling and phosphorus availability along a desert soil chronosequence. Ecology 69:24–39CrossRefGoogle Scholar
  39. Luis P, Kellner H, Zimdars B, Langer U, Martin F, Buscot F (2005) Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microb Ecol 50:570–579PubMedCrossRefGoogle Scholar
  40. Masiello CA, Chadwick OA, Southon J, Torn MS, Harden JW (2004) Weathering controls on mechanisms of carbon storage in grassland soils. Glob Biogeochem Cycles 18:GB4023CrossRefGoogle Scholar
  41. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46:67–83Google Scholar
  42. Mulholland PJ, Rosemond AD (1992) Periphyton response to longitudinal nutrient depletion in a woodland stream: evidence of upstream–downstream linkage. J North Am Benthol Soc 11:405–419CrossRefGoogle Scholar
  43. Neff JC, Gleixner G, Townsend AR (2002) Variable effects of nitrogen addition on the stability and turnover of soil carbon. Nature 419:915–917PubMedCrossRefGoogle Scholar
  44. Nsabimana D, Haynes RJ, Wallis FM (2004) Size, activity and catabolic diversity of the soil microbial biomass as affected by land use. Appl Soil Ecol 26:81–92CrossRefGoogle Scholar
  45. Pennington D, Collins SL (2007) Remotely-sensed response of an aridland ecosystem to pervasive drought. Landsc Ecol 22:897–910CrossRefGoogle Scholar
  46. Rajaniemi TK (2002) Why does fertilization reduce plant species diversity? J Ecol 90:316–324CrossRefGoogle Scholar
  47. Ransom MD, Rice CW, Todd TC, Wehmueller WA (1998) Soils and soil biota. In: Knapp AK, Briggs JM, Hartnett DC, Collins SC (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University, New York, pp 48–66Google Scholar
  48. Saggar S, Tate KR, Feltham CW, Childs CW, Parshotam A (1994) Carbon turnover in a range of allophanic soils amended with 14C-labelled glucose. Soil Biol Biochem 26:1263–1271CrossRefGoogle Scholar
  49. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long-term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  50. Saviozzi A, Levi-Minzi R, Cardelli R, Riffaldi R (2001) A comparison of soil quality in adjacent cultivated, forest and native grassland soils. Plant Soil 233:251–259CrossRefGoogle Scholar
  51. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  52. Schlesinger WH (1977) Carbon balance in terrestrial detritus. Annu Rev Ecol Syst 8:51–81CrossRefGoogle Scholar
  53. Scott-Denton LE, Rosenstiel TN, Monson RK (2005) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Change Biol 11:1–12CrossRefGoogle Scholar
  54. Sinsabaugh RL, Carreiro MM, Alvarez S (2002) Enzyme and microbial dynamics during litter decomposition. In: Burns R (ed) Enzymes in the environment. Dekker, New York, pp 249–266Google Scholar
  55. Sinsabaugh RL, Gallo ME, Lauber C, Waldrop M, Zak DR (2005) Extracellular enzyme activities and soil carbon dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215CrossRefGoogle Scholar
  56. Sponseller RA (2007) Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem. Glob Change Biol 13:426–436CrossRefGoogle Scholar
  57. Stelzer RS, Lamberti GA (2001) Effects of n:P ratio and total nutrient concentration on stream periphyton community structure, biomass, and elemental composition. Limnol Oceanogr 46:356–367CrossRefGoogle Scholar
  58. Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term n deposition in a semiarid grassland. Microb Ecol 51:90–98PubMedCrossRefGoogle Scholar
  59. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to n ferilization. Proc Natl Acad Sci 102:4387–4392PubMedCrossRefGoogle Scholar
  60. Tilman GD (1984) Plant dominance along an experimental nutrient gradient. Ecology 65:1445–1453CrossRefGoogle Scholar
  61. Tobor-Kaplon MA, Bloem J, Romkens PFAM, d Ruiter PC (2005) Functional stability of microbial communities in contaminated soils. Oikos 111:119–129CrossRefGoogle Scholar
  62. Torn MS, Trumbore SE, Chadwick OA, Vitousek PM, Hendricks DM (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173CrossRefGoogle Scholar
  63. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus and atmospheric CO2 in field studies. New Phytol 164:347–355CrossRefGoogle Scholar
  64. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  65. Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36:1443–1451CrossRefGoogle Scholar
  66. Wedin DA, Tilman D (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–1723PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Lydia H. Zeglin
    • 1
    Email author
  • Martina Stursova
    • 1
  • Robert L. Sinsabaugh
    • 1
  • Scott L. Collins
    • 1
  1. 1.Department of Biology, MSC03 2020University of New MexicoAlbuquerqueUSA

Personalised recommendations