, Volume 14, Issue 2, pp 234–247 | Cite as

Indirect Effects of Nitrogen Amendments on Organic Substrate Quality Increase Enzymatic Activity Driving Decomposition in a Mesic Grassland

  • Lisa K. TiemannEmail author
  • Sharon A. Billings


The fate of soil organic carbon (SOC) is determined, in part, by complex interactions between the quality of plant litter inputs, nutrient availability, and the microbial communities that control decomposition rates. This study explores these interactions in a mesic grassland where C and nitrogen (N) availability and plant litter quality have been manipulated using both fertilization and haying for 7 years. We measured a suite of soil parameters including inorganic N, extractable organic C and N (EOC and EON), soil moisture, extracellular enzyme activity (EEA), and the isotopic composition of C and N in the microbial biomass and substrate sources. We use these data to determine how the activity of microbial decomposers was influenced by varying levels of substrate C and N quality and quantity and to explore potential mechanisms explaining the fate of enhanced plant biomass inputs with fertilization. Oxidative EEA targeting relatively recalcitrant C pools was not affected by fertilization. EEA linked to the breakdown of relatively labile C rich substrates exhibited no relationship with inorganic N availability but was significantly greater with fertilization and associated increases in substrate quality. These increases in EEA were not related to an increase in microbial biomass C. The ratio of hydrolytic C:N acquisition enzymes and δ13C and δ15N values of microbial biomass relative to bulk soil C and N, or EOC and EON suggest that microbial communities in fertilized plots were relatively C limited, a feature likely driving enhanced microbial efforts to acquire C from labile sources. These data suggest that in mesic grasslands, enhancements in biomass inputs and quality with fertilization can prompt an increase in EEA within the mineral soil profile with no significant increases in microbial biomass. Our work helps elucidate the microbially mediated fate of enhanced biomass inputs that are greater in magnitude than the associated increases in mineral soil organic matter.


grassland soil organic carbon extracellular enzyme microbial biomass δ13C and δ15microbial substrate quality decomposition Organic matter quality 



Many thanks to R. Rastok, A. Reed, R. Russell, C. Murphy, B. Johanning, G. Pittman, S. Hinman and Dr. Bryan Foster. We also thank two anonymous reviewers for comments that greatly improved the manuscript. Support was provided by NSF EPS-0553722, a contract with Kansas Technology Enterprise Corporation, KU’s General Research Fund allocation, and the U.S. Department of Energy’s National Institute of Climate Change Research (NICCR). This represents University of Kansas Field Station publication number 905.


  1. 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 31:769–77.CrossRefGoogle Scholar
  2. Asner GP, Seastedt TR, Townsend AR. 1997. The decoupling of terrestrial carbon and nitrogen cycles. Bioscience 47:226–34.CrossRefGoogle Scholar
  3. Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC. 1999. Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–30.CrossRefGoogle Scholar
  4. Billings SA. 2006. Soil organic matter dynamics and land use change at a grassland/forest ecotone. Soil Biol Biochem 38:2934–43.CrossRefGoogle Scholar
  5. Billings SA, Brewer CM, Foster BL. 2006. Incorporation of plant residues into soil organic matter fractions with grassland management practices in the North American Midwest. Ecosystems 9:805–15.CrossRefGoogle Scholar
  6. Billings SA, Gaydess EA. 2008. Soil nitrogen and carbon dynamics in a fragmented landscape experiencing forest succession. Landscape Ecol 23:581–93.CrossRefGoogle Scholar
  7. Brookes PC, Landman A, Pruden G, Jenkinson DS. 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–42.CrossRefGoogle Scholar
  8. Bridgham SD, Pastor J, McClaugherty CA, Richardson CJ. 1995. Nutrient-use efficiency: a litterfall index, a model, and a test along a nutrient-availability gradient in North Carolina peatlands. Am Nat 145:1–21.CrossRefGoogle Scholar
  9. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF. 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–65.CrossRefGoogle Scholar
  10. Chapin FS, Matson PA, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. New York (NY): Springer. p 436.Google Scholar
  11. Conant RT, Paustian K, Elliott ET. 2001. Grassland management and conversion into grassland: effects on soil carbon. Ecol Appl 11:343–55.CrossRefGoogle Scholar
  12. Conant RT, Paustian K, Del Grosso SJ, Parton WJ. 2005. Nitrogen pools and fluxes in grassland soils sequestering carbon. Nutr Cycl Agroecosyst 71:239–48.CrossRefGoogle Scholar
  13. Coyle JS, Dijkstra P, Doucett RR, Schwartz E, Hart SC, Hungate BA. 2009. Relationships between C and N availability, substrate age, and natural abundance 13C and 15N signatures of soil microbial biomass in a semiarid climate. Soil Biol Biochem 41:1605–11.CrossRefGoogle Scholar
  14. Dijkstra FA, Hobbie SE, Knops JMH, Reich PB. 2004. Nitrogen deposition and plant species interact to influence soil carbon stabilization. Ecol Lett 7:1192–8.CrossRefGoogle Scholar
  15. Dijkstra FA, Ishizu A, Doucett R, Hart SC, Schwartz E, Menyailo OV, Hungate BA. 2006. 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–66.CrossRefGoogle Scholar
  16. Dijkstra FA, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA. 2008. 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–97.PubMedCrossRefGoogle Scholar
  17. Doyle A, Weintraub MN, Schimel JP. 2004. Persulfate digest and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci Soc Am 68:669–76.CrossRefGoogle Scholar
  18. Ehleringer JR, Buchmann N, Flanagan LB. 2000. Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–22.CrossRefGoogle Scholar
  19. Fierer N, Bradford MA, Jackson RB. 2007. Towards an ecological classification of soil bacteria. Ecology 88:1354–64.PubMedCrossRefGoogle Scholar
  20. Fog K. 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–62.CrossRefGoogle Scholar
  21. Foster BL, Dickson TL. 2004. Grassland diversity and productivity: the interplay of resource availability and propagule pools. Ecology 85:1541–7.CrossRefGoogle Scholar
  22. Foster BL, Kindscher K, Houseman GR, Murphy CA. 2009. Effects of hay management and native species sowing on grassland community structure, biomass and restoration. Ecol Appl 19:1884–96.PubMedCrossRefGoogle Scholar
  23. Franzluebbers AJ, Stuedemann JA. 2005. Bermudagrass management in the southern piedmont USA: VII. Soil-profile organic carbon and total nitrogen. Soil Sci Soc Am 69:1455–62.CrossRefGoogle Scholar
  24. Frey SD, Gupta VVSR, Elliot ET, Paustian K. 2001. Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biol Biochem 33:1759–68.CrossRefGoogle Scholar
  25. Gallo ME, Lauber CL, Cabaniss SE, Waldrop MP, Sinsabaugh RL, Zak DR. 2005. Soil organic matter and litter chemistry response to experimental N deposition in northern temperate deciduous forest ecosystems. Glob Change Biol 11:1514–21.CrossRefGoogle Scholar
  26. Garcia FO, Rice CW. 1994. Microbial biomass dynamics in tallgrass prairie. Soil Sci Soc Am J 58:816–23.CrossRefGoogle Scholar
  27. Hobbie SE. 2000. Interactions between litter lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest. Ecosystems 3:484–94.CrossRefGoogle Scholar
  28. Hobbie SE. 2005. Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 8:644–56.CrossRefGoogle Scholar
  29. High Plains Regional Climate Center (HPRCC). Historical Climate Data Summaries. Accessed [11/17/2007].
  30. Jenkinson DS, Brookes PC, Powlson DS. 2004. Measuring soil microbial biomass. Soil Biol Biochem 36:5–7.CrossRefGoogle Scholar
  31. Jones SK, Rees RM, Skiba UM, Ball BC. 2005. Greenhouse gas emissions from managed grassland. Global Planet Change 47:201–11.CrossRefGoogle Scholar
  32. Knorr M, Frey SD, Curtis PS. 2005. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–7.CrossRefGoogle Scholar
  33. Lee BL, Lorenz N, Dick LK, Dick RP. 2007. Cold storage and pretreatment incubation effects on soil microbial properties. Soil Sci Soc Am 71:1299–305.CrossRefGoogle Scholar
  34. Lovell RD, Jarvis SC, Bardgett RD. 1995. Soil microbial biomass and activity in long-term grassland—effects of management changes. Soil Biol Biochem 27:969–75.CrossRefGoogle Scholar
  35. Malhi SS, Nyborg M, Harapiak JT, Heier K, Flore NA. 1997. Increasing organic C and N under bromegrass with long-term N fertilization. Nutr Cycl Agroecosyst 49:255–60.CrossRefGoogle Scholar
  36. McCulley RM, Burke IC, Nelson JA, Lauenroth WK, Knapp AK, Kelly EF. 2005. Regional patterns in carbon cycling across the Great Plains of North America. Ecosystems 8:106–21.CrossRefGoogle Scholar
  37. Mosier AR, Parton WJ, Phongpan S. 1998. Long-term large N and immediate small N addition effects on trace gas fluxes in the Colorado shortgrass steppe. Biol Fertil Soils 28:44–50.CrossRefGoogle Scholar
  38. Natural Resources Conservation Service (NRCS), United States Department of Agriculture. Web Soil Survey. Accessed [10/23/2007].
  39. Neff JC, Townsend AR, Gleixnerk G, Lehman SJ, Turnbull J, Bowman WD. 2002. Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–17.PubMedCrossRefGoogle Scholar
  40. 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 34:1309–15.CrossRefGoogle Scholar
  41. Schlesinger WH. 1997. Biogeochemistry: an analysis of global change. San Diego (CA): Academic Press. p 588.Google Scholar
  42. Sinsabaugh RL, Carreiro MM, Repert DA. 2002. Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24.CrossRefGoogle Scholar
  43. Sinsabaugh RL, Zak DR, Gallo M, Lauber C, Amonette R. 2004. Nitrogen deposition and dissolved organic carbon production in northern temperate forests. Soil Biol Biochem 36:1509–15.CrossRefGoogle Scholar
  44. Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MA, Zak DR. 2005. Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–15.CrossRefGoogle Scholar
  45. Stursova M, Crenshaw CL, Sinsabaugh RL. 2006. Microbial response to long-term N deposition in a semiarid grassland. Microb Ecol 51:90–8.PubMedCrossRefGoogle Scholar
  46. Tiemann LK, Billings SA. 2008. Carbon controls on nitrous oxide production with changes in substrate availability in a North American grassland. Soil Sci 173:332–41.CrossRefGoogle Scholar
  47. Vitousek P. 1982. Nutrient cycling and nutrient use efficiency. Am Nat 119:553–72.CrossRefGoogle Scholar
  48. Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C. 2004. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–7.CrossRefGoogle Scholar
  49. Well R, Kurganova I, de Gerenyu VL, Flessa H. 2006. Isotopomer signatures of soil-emitted N2O under different moisture conditions–A microcosm study with arable loess soil. Soil Biol Biochem 38:2923–33.CrossRefGoogle Scholar
  50. Zeglin LH, Stursova M. 2007. Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 154:349–59.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Ecology and Evolutionary BiologyUniversity of KansasLawrenceUSA
  2. 2.University of Kansas and Kansas Biological SurveyLawrenceUSA

Personalised recommendations