, Volume 102, Issue 1–3, pp 31–43 | Cite as

Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse

  • Robert L. SinsabaughEmail author
  • Jennifer J. Follstad Shah
Synthesis & Emerging Ideas


The flow of carbon and nutrients from plant production into detrital food webs is mediated by microbial enzymes released into the environment (ecoenzymes). Ecoenzymatic activities are linked to both microbial metabolism and environmental resource availability. In this paper, we extend the theoretical and empirical framework for ecoenzymatic stoichiometry from nutrient availability to carbon composition by relating ratios of β-1,4-glucosidase (BG), acid (alkaline) phosphatase (AP), β-N-acetylglucosaminidase (NAG), leucine aminopeptidase (LAP) and phenol oxidase (POX) activities in soils to measures of organic matter recalcitrance, using data from 28 ecosystems. BG and POX activities are uncorrelated even though both are required for lignocellulose degradation. However, the ratio of BG:POX activity is negatively correlated with the relative abundance of recalcitrant carbon. Unlike BG, POX activity is positively correlated with (NAG + LAP) and AP activities. We propose that the effect of organic matter recalcitrance on microbial C:N and C:P threshold element ratios (TER) can be represented by normalizing BG, AP and (NAG + LAP) activities to POX activity. The scaling relationships among these ratios indicate that the increasing recalcitrance of decomposing organic matter effectively reverses the growth rate hypothesis of stoichiometric theory by decreasing carbon and nutrient availability and slowing growth, which increases TERN:P. This effect is consistent with the narrow difference between the mean elemental C:N ratios of soil organic matter and microbial biomass and with the inhibitory effect of N enrichment on rates of decomposition and microbial metabolism for recalcitrant organic matter. From these findings, we propose a conceptual framework for bottom-up decomposition models that integrate the stoichiometry of ecoenzymatic activities into general theories of ecology.


β-glucosidase β-N-acetylglucosaminidase Decomposition Ecological stoichiometry Extracellular enzyme activity Leucine aminopeptidase Phenol oxidase Phosphatase Soil organic matter Threshold element ratio 



Assimilation efficiency for nitrogen


Assimilation efficiency for phosphorus


Acid (alkaline) phosphatase


Biomass C:N ratio


Biomass C:P ratio




Ecoenzymatic activity


Leucine aminopeptidase




Phenol oxidase


Soil organic matter


Threshold element ratio


Growth efficiency



J.J.F.S. was supported by the National Science Foundation (DBI-0630558). R.L.S. was supported by NSF EaGER (DEB-0946288) and Ecosystem Studies programs (DEB-0918718). Source data were contributed by Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop M, Wallenstein M, Zak DR, Zeglin LH.


  1. Abe T, Watanabe A (2004) X-ray photoelectron spectroscopy of nitrogen functional groups in soil humic acids. Soil Sci 169:35–43CrossRefGoogle Scholar
  2. Allen AP, Gillooly JF (2009) Towards and integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384CrossRefGoogle Scholar
  3. Allison SD (2006) Brown ground: a soil carbon analogue for the green world hypothesis? Am Nat 167:619–627CrossRefGoogle Scholar
  4. Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256CrossRefGoogle Scholar
  5. Allison SD, Vitousek PM (2004) Extracellular enzymes and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica 36:285–296Google Scholar
  6. Allison SD, Gartner T, Holland K, Weintraub M, Sinsabaugh RL (2007) Soil enzymes: linking proteomics and ecological process. Manual of environmental microbiology. ASM Press, Washington, pp 704–711Google Scholar
  7. Artigas J, Romani AM, Sabater S (2008) Relating nutrient molar ratios of attached microbial communites to organic matter utilization in forested streams. Arch für Hydrobiol 173:255–264Google Scholar
  8. Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbol Rev 30:215–242CrossRefGoogle Scholar
  9. Berg B, McClaugherty C (2003) Plant litter decomposition, humus formation, carbon sequestration. Springer Verlag, BerlinGoogle Scholar
  10. Bossata E, Ågren GI (1999) Soil organic matter quality interpreted themodynamically. Soil Biol Biochem 31:1889–1891CrossRefGoogle Scholar
  11. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  12. Burke RM, Cairney JWG (2002) Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 12:105–116CrossRefGoogle Scholar
  13. 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
  14. Claus H (2003) Laccases and their occurence in prokaryotes. Arch Microbiol 179:145–150Google Scholar
  15. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  16. Conant RT, Drijber RA, Haddix ML, Parton WJ, Paul EA, Plante AF, Six J, Steinweg JM (2008a) Sensitivity of organic matter decomposition to warming varies with its quality. Global Change Biol 14:868–877CrossRefGoogle Scholar
  17. Conant RT, Steinweg JM, Haddix ML, Paul EA, Plante AF, Six J (2008b) Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance. Ecology 89:2384–2391CrossRefGoogle Scholar
  18. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182:736–750CrossRefGoogle Scholar
  19. Danger M, Daufresne T, Lucas F, Pissard S, Lacroix G (2008) Does Liebig’s law of the minimum scale up from species to communities? Oikos 117:1741–1751CrossRefGoogle Scholar
  20. DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Anthropogenic NO3-deposition alters microbial community function in northern hardwood forests. Soil Sci Soc Am J 68:132–138Google Scholar
  21. Doi H, Cherif M, Iwabuchi T, Katano I, Stegen JC, Striebel M (2010) Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119:752–765CrossRefGoogle Scholar
  22. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie SE, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943CrossRefGoogle Scholar
  23. Eriksson K-E, Blanchette RA, Ander P (1990) Microbial and enzymatic degradation of wood components. Springer-Verlag, BerlinGoogle Scholar
  24. Fierer N, Craine JM, McLauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326CrossRefGoogle Scholar
  25. Fog K (1988) The effect of added nitrogen on the rate of decomposition organic matter. Biol Rev 63:433–462CrossRefGoogle Scholar
  26. Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, Yoshida T (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779CrossRefGoogle Scholar
  27. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307CrossRefGoogle Scholar
  28. Grandy AS, Neff JC, Weintraub MN (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711CrossRefGoogle Scholar
  29. Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49CrossRefGoogle Scholar
  30. Gregorich EG, Beare MH, Mckim UF, Skjemstad JO (2006) Chemical and biological characteristics of physically uncomplexed organic matter. Soil Sci Soc Am J 70:975–985CrossRefGoogle Scholar
  31. Gusewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219CrossRefGoogle Scholar
  32. Hammel KE (1997) Fungal degradation of lignin. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, UK, pp 33–46Google Scholar
  33. Herman J, Moorhead D, Bjorn B (2008) The relationship between rates of lignin and cellulose decay in aboveground litter. Soil Biol Biochem 40:2620–2626CrossRefGoogle Scholar
  34. Higuchi T (1990) Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24:23–63CrossRefGoogle Scholar
  35. Hill BH, Elonen CM, Jicha TM, Bolgrien DW, Moffett MF (2009) Sediment microbial enzyme activity as an indicator of nutrient limitation in the great rivers of the Upper Mississippi River basin. Biogeochemistry. doi: 10.1007/s10533-009-9366-0
  36. Hladyz S, Gessner MO, Giller PS, Pozo J, Woodward G (2009) Resource quality and stoichiometric constraints on stream ecosystem functioning. Freshw Biol 54:957–970CrossRefGoogle Scholar
  37. Hobbie EA, Horton TR (2007) Evidence that saprotrophic fungi mobilise carbon and mycorrhizal fungi mobilise nitrogen during litter decomposition. New Phytol 173:447–449CrossRefGoogle Scholar
  38. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257CrossRefGoogle Scholar
  39. Ljungdahl LG, Eriksson K-E (1985) Ecology of microbial cellulose degradation. Adv Microb Ecol 8:237–299Google Scholar
  40. Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472CrossRefGoogle Scholar
  41. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  42. Michel K, Matzner E (2003) Response of enzyme activities to nitrogen addition in forest floors of different C-to-N ratios. Biol Fertil Soils 38:102–109CrossRefGoogle Scholar
  43. Moore TR, Trofymow JA, Prescott CE, Fyles J, Titus BD (2006) Patterns of carbon, nitrogen and phosphorus dynamics in decomposing foliar litter in Canadian forests. Ecosystems 9:46–62CrossRefGoogle Scholar
  44. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  45. Nannipieri P, Paul E (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369CrossRefGoogle Scholar
  46. Nierop KGJ, Preston CM, Verstraten JM (2006) Linking the B ring hydroxylation pattern of condensed tannins to C, N and P mineralization. A case study using four tannins. Soil Biol Biochem 38:2794–2802CrossRefGoogle Scholar
  47. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190CrossRefGoogle Scholar
  48. Osono T, Takeda H (2004) Accumulation and release of nitrogen and phosphorus in relation to lignin decomposition in leaf litter of 14 tree species. Ecol Res 19:593–602CrossRefGoogle Scholar
  49. Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long term decomposition. Science 315:361–362CrossRefGoogle Scholar
  50. Rabinovich ML, Bolobova AV, Vasilchenko LG (2004) Fungal decomposition of natural aromatic structures and xenobiotics: a review. Appl Biochem Microbiol 40:1–17CrossRefGoogle 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. Schulten HR, Leinweber P (2000) New insights into organic-mineral particles: composition, properties and models of molecular structure. Biol Fertil Soils 30:399–432CrossRefGoogle Scholar
  53. Sinsabaugh RL (2005) Fungal enzymes at the community scale. In: Dighton J, Oudermans P, White J (eds) The fungal community, 3rd edn, Chap 17. CRC Press, New YorkGoogle Scholar
  54. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  55. Sinsabaugh RL, Foreman CM (2001) Activity profiles of bacterioplankton in a eutrophic river. Freshw Biol 46:1–12CrossRefGoogle Scholar
  56. Sinsabaugh RL, Linkins AE (1987) Inhibition of the Trichoderma viride cellulase complex by leaf litter extracts. Soil Biol Biochem 19:719–725CrossRefGoogle Scholar
  57. Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  58. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop M, Wallenstein M, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264Google Scholar
  59. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798CrossRefGoogle Scholar
  60. Sinsabaugh RL, Van Horn DE, Follstad Shah JJ, Findlay SG (2010) Ecoenzymatic stoichiometry in relation to productivity for freshwater biofilm and plankton communities. Microb Ecol (in press)Google Scholar
  61. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University, PrincetonGoogle Scholar
  62. Stursova M, Crenshaw C, Sinsabaugh RL (2006) Microbial responses to long term N deposition in a semi-arid grassland. Microb Ecol 51:90–98CrossRefGoogle Scholar
  63. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963CrossRefGoogle Scholar
  64. Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70:91–104Google Scholar
  65. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120CrossRefGoogle Scholar
  66. Warton DI, Wright J, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Robert L. Sinsabaugh
    • 1
    Email author
  • Jennifer J. Follstad Shah
    • 2
  1. 1.Biology DepartmentUniversity of New MexicoAlbuquerqueUSA
  2. 2.Biology DepartmentDuke UniversityDurham27708USA

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