, Volume 163, Issue 4, pp 1069–1078 | Cite as

Amino acid abundance and proteolytic potential in North American soils

  • Kirsten S. Hofmockel
  • Noah Fierer
  • Benjamin P. Colman
  • Robert B. Jackson
Ecosystem ecology - Original Paper


Studies of nitrogen (N) cycling have traditionally focused on N mineralization as the primary process limiting plant assimilation of N. Recent evidence has shown that plants may assimilate amino acids (AAs) directly, circumventing the mineralization pathway. However, the general abundance of soil AAs and their relative importance in plant N uptake remains unclear in most ecosystems. We compared the concentrations and potential production rates of AAs and NH4 +, as well as the edaphic factors that influence AA dynamics, in 84 soils across the United States. Across all sites, NH4 + and AA-N comprised similar proportions of the total bioavailable N pool (~20%), with NO3 being the dominant form of extractable N everywhere but in tundra and boreal forest soils. Potential rates of AA production were at least comparable to those of NH4 + production in all ecosystems, particularly in semi-arid grasslands, where AA production rates were six times greater than for NH4 + (P < 0.01). Potential rates of proteolytic enzyme activity were greatest in bacteria-dominated soils with low NH4 + concentrations, including many grassland soils. Based on research performed under standardized laboratory conditions, our continental-scale analyses suggest that soil AA and NH4 + concentrations are similar in most soils and that AAs may contribute to plant and microbial N demand in most ecosystems, particularly in ecosystems with N-poor soils.


Soil N cycle Proteolysis Ammonium Amino acid Organic N Nitrification Nitrogen mineralization Protein mineralization 



We thank Rebecca McCulley for comments that greatly improved the manuscript, and Sean Berthrong and Isabel Heine for lab assistance. We are also grateful to the many people who generously collected field samples for this study. Support for this work was provided by a NSF Postdoctoral Fellowship to NF and by grants from NIGEC/NICCR (through the office of Biological and Environmental Research at the Department of Energy) and the National Science Foundation (DEB 02-35425 and 07-17191) to RBJ.

Supplementary material

442_2010_1601_MOESM1_ESM.doc (209 kb)
Supplementary material 1 (DOC 209 kb)


  1. Austin AT, Sala OE, Jackson RB (2006) Inhibition of nitrification alters carbon turnover in the Patagonian steppe. Ecosystems 9:1257–1265CrossRefGoogle Scholar
  2. Baath E (1996) Adaptation of soil bacterial communities to prevailing pH in different soils. FEMS Microbiol Ecol 19:227–237Google Scholar
  3. Baath E (1998) Growth rates of bacterial communities in soils at varying pH: a comparison of the thymidine and leucine incorporation techniques. Microb Ecol 36:316–327CrossRefPubMedGoogle Scholar
  4. Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287CrossRefGoogle Scholar
  5. Barrett JE, Burke IC (2000) Potential nitrogen immobilization in grassland soils across a soil organic matter gradient. Soil Biol Biochem 32:1707–1716CrossRefGoogle Scholar
  6. Berthrong ST, Finzi AC (2006) Amino acid cycling in three cold-temperate forests of the northeastern USA. Soil Biol Biochem 38:861–869CrossRefGoogle Scholar
  7. Coffman JA, Cooper TG (1997) Nitrogen GATA factors participate in transcriptional regulation of vacuolar protease genes in Saccharomyces cerevisiae. J Bacteriol 179:5609–5613Google Scholar
  8. Crenshaw CL, Lauber C, Sinsabaugh RL, Stavely LK (2008) Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 87:17–27CrossRefGoogle Scholar
  9. de Vries FT, Hoffland E, van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38:2092–2103CrossRefGoogle Scholar
  10. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631CrossRefPubMedGoogle Scholar
  11. Fierer N, Craine JM, McLauchlan K, Schimel JP (2005a) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326CrossRefGoogle Scholar
  12. Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005b) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120CrossRefPubMedGoogle Scholar
  13. Fierer N, Colman BP, Schimel JP, Jackson RB (2006) Predicting the temperature dependence of microbial respiration in soil: a continental-scale analysis. Global Biogeochem Cycles 20:10CrossRefGoogle Scholar
  14. Finzi AC, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86:3345–3353CrossRefGoogle Scholar
  15. Fuller ME, Scow KM (1996) Effects of toluene on microbially-mediated processes involved in the soil nitrogen cycle. Microb Ecol 32:171–184CrossRefPubMedGoogle Scholar
  16. Green LE, Porras-Alfaro A, Sinsabaugh RL (2008) Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. J Ecol 96:1076–1085CrossRefGoogle Scholar
  17. Gulledge J, Schimel JP (1998) Moisture control over atmospheric CH4 consumption and CO2 production in diverse Alaskan soils. Soil Biol Biochem 30:1127–1132CrossRefGoogle Scholar
  18. Hayano K (1996) Characterization and origin of protease activity in cultivated soils. Jpn Agric Res Q 30:79–84Google Scholar
  19. Hobbie JE, Hobbie EA, Drossman H, Conte M, Weber JC, Shamhart J, Weinrobe M (2009) Mycorrhizal fungi supply nitrogen to host plants in Arctic tundra and boreal forests: 15N is the key signal. Can J Microbiol 55:84–94CrossRefPubMedGoogle Scholar
  20. Hofmockel KS, Schlesinger WH, Jackson RB (2007) Effects of elevated atmospheric carbon dioxide on amino acid and NH4 +-N cycling in a temperate pine ecosystem. Global Change Biol 13:1950–1959CrossRefGoogle Scholar
  21. Jan MT, Roberts P, Tonheim SK, Jones DL (2009) Protein breakdown represents a major bottleneck in nitrogen cycling in grassland soils. Soil Biol Biochem 41:2272–2282CrossRefGoogle Scholar
  22. Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219CrossRefGoogle Scholar
  23. Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34:1893–1902CrossRefGoogle Scholar
  24. Jones DL, Shannon D, Murphy DV, Farrar JF (2004) Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biol Biochem 36:749–756CrossRefGoogle Scholar
  25. Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol Biochem 37:413–423CrossRefGoogle Scholar
  26. Jones DL, Kielland K, Sinclair FL, Dahlgren RA, Newsham KK, Farrar JF, Murphy DV (2009) Soil organic nitrogen mineralization across a global latitudinal gradient. Global Biogeochem Cycles 23:GB1016CrossRefGoogle Scholar
  27. Kielland K (1994) Amino-acid-absorption by arctic plants—implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383CrossRefGoogle Scholar
  28. Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98CrossRefGoogle Scholar
  29. Kielland K, McFarland JW, Ruess RW, Olson K (2007) Rapid cycling of organic nitrogen in taiga forest ecosystems. Ecosystems 10:360–368CrossRefGoogle Scholar
  30. Ladd JN (1972) Properties of proteolytic enzymes extracted from soil. Soil Biol Biochem 4:227–237CrossRefGoogle Scholar
  31. Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316CrossRefGoogle Scholar
  32. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631CrossRefGoogle Scholar
  33. Liu PV, Hsieh HC (1969) Inhibition of protease production of various bacteria by ammonium salts—its effect on toxin production and virulence. J Bacteriol 99:406Google Scholar
  34. McFarland JW, Ruess RW, Kielland K, Doyle AP (2002) Cycling dynamics of NH4 + and amino acid nitrogen in soils of a deciduous boreal forest ecosystem. Ecosystems 5:775–788Google Scholar
  35. Näsholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, Hogberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916CrossRefGoogle Scholar
  36. Nordin A, Hogberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132CrossRefGoogle Scholar
  37. Sakurai M, Suzuki K, Onodera M, Shinano T, Osaki M (2007) Analysis of bacterial communities in soil by PCR-DGGE targeting protease genes. Soil Biol Biochem 39:2777–2784CrossRefGoogle Scholar
  38. Santiago LS, Schuur EAG, Silvera K (2005) Nutrient cycling and plant-soil feedbacks along a precipitation gradient in lowland Panama. J Trop Ecol 21:461–470CrossRefGoogle Scholar
  39. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  40. Schimel JP, Jackson LE, Firestone MK (1989) Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a California annual grassland. Soil Biol Biochem 21:1059–1066CrossRefGoogle Scholar
  41. Schulten HR, Schnitzer M (1998) The chemistry of soil organic nitrogen: a review. Biol Fertil Soils 26:1–15CrossRefGoogle Scholar
  42. Skujins J (1967) Enzymes in soil. In: McLaren AD, Peterson GH (eds) Soil biochemistry, vol 1. Marcel Dekker, New York, pp 371–414Google Scholar
  43. Stursova M, Sinsabaugh RL (2008) Stabilization of oxidative enzymes in desert soil may limit organic matter accumulation. Soil Biol Biochem 40:550–553CrossRefGoogle Scholar
  44. Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51:90–98CrossRefPubMedGoogle Scholar
  45. Tabatabai MA (1995) Enzymes. In: Weaver RW, Augle S, Bottomly PJ, Bezdicek D, Smith S, Tabatabai A, Wollum A (eds) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 775–833Google Scholar
  46. Watanabe K, Hayano K (1995) Seasonal-variation of soil protease activities and their relation to proteolytic bacteria and Bacillus spp. in paddy field soil. Soil Biol Biochem 27:197–203CrossRefGoogle Scholar
  47. Watanabe K, Sakai J, Hayano K (2003) Bacterial extracellular protease activities in field soils under different fertilizer managements. Can J Microbiol 49:305–312CrossRefPubMedGoogle Scholar
  48. Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635CrossRefPubMedGoogle Scholar
  49. Weintraub MN, Schimel JP (2005) Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biol Biochem 37:1469–1475CrossRefGoogle Scholar
  50. Zak DR, Grigal DF, Ohmann LF (1993) Kinetics of microbial respiration and nitrogen mineralization in Great-Lakes forests. Soil Sci Soc Am J 57:1100–1106CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Kirsten S. Hofmockel
    • 1
    • 2
  • Noah Fierer
    • 3
    • 4
  • Benjamin P. Colman
    • 5
    • 6
  • Robert B. Jackson
    • 1
    • 6
  1. 1.Nicholas School of the Environment and Earth SciencesDuke UniversityDurhamUSA
  2. 2.Department of Ecology, Evolution and Organismal BiologyIowa State UniversityAmesUSA
  3. 3.Cooperative Institute for Research in Environmental SciencesUniversity of Colorado at BoulderBoulderUSA
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of Colorado at BoulderBoulderUSA
  5. 5.Department of Ecology, Evolution, and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  6. 6.Department of BiologyDuke UniversityDurhamUSA

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