Skip to main content
SpringerLink
Log in

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

  • Synthesis & Emerging Ideas
  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AN :

Assimilation efficiency for nitrogen

AP :

Assimilation efficiency for phosphorus

AP:

Acid (alkaline) phosphatase

BC:N :

Biomass C:N ratio

BC:P :

Biomass C:P ratio

BG:

β-1,4-glucosidase

EEA:

Ecoenzymatic activity

LAP:

Leucine aminopeptidase

NAG:

β-N-acetylglucosaminidase

POX:

Phenol oxidase

SOM:

Soil organic matter

TER:

Threshold element ratio

GE:

Growth efficiency

References

  • Abe T, Watanabe A (2004) X-ray photoelectron spectroscopy of nitrogen functional groups in soil humic acids. Soil Sci 169:35–43

    Article  Google Scholar 

  • Allen AP, Gillooly JF (2009) Towards and integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384

    Article  Google Scholar 

  • Allison SD (2006) Brown ground: a soil carbon analogue for the green world hypothesis? Am Nat 167:619–627

    Article  Google Scholar 

  • Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2004) Extracellular enzymes and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica 36:285–296

    Google Scholar 

  • 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 704–711

    Google Scholar 

  • 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 173:255–264

    Google Scholar 

  • Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbol Rev 30:215–242

    Article  Google Scholar 

  • Berg B, McClaugherty C (2003) Plant litter decomposition, humus formation, carbon sequestration. Springer Verlag, Berlin

    Google Scholar 

  • Bossata E, Ågren GI (1999) Soil organic matter quality interpreted themodynamically. Soil Biol Biochem 31:1889–1891

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Burke RM, Cairney JWG (2002) Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 12:105–116

    Article  Google Scholar 

  • Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Claus H (2003) Laccases and their occurence in prokaryotes. Arch Microbiol 179:145–150

    Google Scholar 

  • Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • 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 14:868–877

    Article  Google Scholar 

  • 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 89:2384–2391

    Article  Google Scholar 

  • 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 182:736–750

    Article  Google Scholar 

  • 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 117:1741–1751

    Article  Google Scholar 

  • 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 68:132–138

    Google Scholar 

  • 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 119:752–765

    Article  Google Scholar 

  • 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 6:936–943

    Article  Google Scholar 

  • Eriksson K-E, Blanchette RA, Ander P (1990) Microbial and enzymatic degradation of wood components. Springer-Verlag, Berlin

    Google Scholar 

  • Fierer N, Craine JM, McLauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326

    Article  Google Scholar 

  • Fog K (1988) The effect of added nitrogen on the rate of decomposition organic matter. Biol Rev 63:433–462

    Article  Google Scholar 

  • 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 9:774–779

    Article  Google Scholar 

  • 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 404:297–307

    Article  Google Scholar 

  • Grandy AS, Neff JC, Weintraub MN (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711

    Article  Google Scholar 

  • 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 91:37–49

    Article  Google Scholar 

  • Gregorich EG, Beare MH, Mckim UF, Skjemstad JO (2006) Chemical and biological characteristics of physically uncomplexed organic matter. Soil Sci Soc Am J 70:975–985

    Article  Google Scholar 

  • Gusewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  • 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 33–46

    Google Scholar 

  • Herman J, Moorhead D, Bjorn B (2008) The relationship between rates of lignin and cellulose decay in aboveground litter. Soil Biol Biochem 40:2620–2626

    Article  Google Scholar 

  • Higuchi T (1990) Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24:23–63

    Article  Google Scholar 

  • 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

  • Hladyz S, Gessner MO, Giller PS, Pozo J, Woodward G (2009) Resource quality and stoichiometric constraints on stream ecosystem functioning. Freshw Biol 54:957–970

    Article  Google Scholar 

  • Hobbie EA, Horton TR (2007) Evidence that saprotrophic fungi mobilise carbon and mycorrhizal fungi mobilise nitrogen during litter decomposition. New Phytol 173:447–449

    Article  Google Scholar 

  • Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257

    Article  Google Scholar 

  • Ljungdahl LG, Eriksson K-E (1985) Ecology of microbial cellulose degradation. Adv Microb Ecol 8:237–299

    Google Scholar 

  • Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472

    Article  Google Scholar 

  • Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626

    Article  Google Scholar 

  • Michel K, Matzner E (2003) Response of enzyme activities to nitrogen addition in forest floors of different C-to-N ratios. Biol Fertil Soils 38:102–109

    Article  Google Scholar 

  • 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 9:46–62

    Article  Google Scholar 

  • Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174

    Article  Google Scholar 

  • Nannipieri P, Paul E (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369

    Article  Google Scholar 

  • 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 38:2794–2802

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    Article  Google Scholar 

  • 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 19:593–602

    Article  Google Scholar 

  • 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 315:361–362

    Article  Google Scholar 

  • Rabinovich ML, Bolobova AV, Vasilchenko LG (2004) Fungal decomposition of natural aromatic structures and xenobiotics: a review. Appl Biochem Microbiol 40:1–17

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  Google Scholar 

  • Schulten HR, Leinweber P (2000) New insights into organic-mineral particles: composition, properties and models of molecular structure. Biol Fertil Soils 30:399–432

    Article  Google Scholar 

  • 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 York

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  Google Scholar 

  • Sinsabaugh RL, Foreman CM (2001) Activity profiles of bacterioplankton in a eutrophic river. Freshw Biol 46:1–12

    Article  Google Scholar 

  • Sinsabaugh RL, Linkins AE (1987) Inhibition of the Trichoderma viride cellulase complex by leaf litter extracts. Soil Biol Biochem 19:719–725

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 11:1252–1264

    Google Scholar 

  • Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    Article  Google Scholar 

  • 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)

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University, Princeton

    Google Scholar 

  • Stursova M, Crenshaw C, Sinsabaugh RL (2006) Microbial responses to long term N deposition in a semi-arid grassland. Microb Ecol 51:90–98

    Article  Google Scholar 

  • 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 22:955–963

    Article  Google Scholar 

  • Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70:91–104

    Google Scholar 

  • Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120

    Article  Google Scholar 

  • Warton DI, Wright J, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Biology Department, University of New Mexico, Albuquerque, NM, 87131, USA

    Robert L. Sinsabaugh

  2. Biology Department, Duke University, Durham, NC, 27708, USA

    Jennifer J. Follstad Shah

Authors
  1. Robert L. Sinsabaugh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer J. Follstad Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert L. Sinsabaugh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sinsabaugh, R.L., Follstad Shah, J.J. Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102, 31–43 (2011). https://doi.org/10.1007/s10533-010-9482-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-010-9482-x

Keywords

Search

Navigation