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Extracellular enzyme kinetics scale with resource availability

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Abstract

Microbial community metabolism relies on external digestion, mediated by extracellular enzymes that break down complex organic matter into molecules small enough for cells to assimilate. We analyzed the kinetics of 40 extracellular enzymes that mediate the degradation and assimilation of carbon, nitrogen and phosphorus by diverse aquatic and terrestrial microbial communities (1160 cases). Regression analyses were conducted by habitat (aquatic and terrestrial), enzyme class (hydrolases and oxidoreductases) and assay methodology (low affinity and high affinity substrates) to relate potential reaction rates to substrate availability. Across enzyme classes and habitats, the scaling relationships between apparent Vmax and apparent Km followed similar power laws with exponents of 0.44 to 0.67. These exponents, called elasticities, were not statistically distinct from a central value of 0.50, which occurs when the Km of an enzyme equals substrate concentration, a condition optimal for maintenance of steady state. We also conducted an ecosystem scale analysis of ten extracellular hydrolase activities in relation to soil and sediment organic carbon (2,000–5,000 cases/enzyme) that yielded elasticities near 1.0 (0.9 ± 0.2, n = 36). At the metabolomic scale, the elasticity of extracellular enzymatic reactions is the proportionality constant that connects the C:N:P stoichiometries of organic matter and ecoenzymatic activities. At the ecosystem scale, the elasticity of extracellular enzymatic reactions shows that organic matter ultimately limits effective enzyme binding sites. Our findings suggest that one mechanism by which microbial communities maintain homeostasis is regulating extracellular enzyme expression to optimize the short-term responsiveness of substrate acquisition. The analyses also show that, like elemental stoichiometry, the fundamental attributes of enzymatic reactions can be extrapolated from biochemical to community and ecosystem scales.

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Acknowledgments

RLS acknowledges support from the NSF Ecosystem Sciences program (DEB-0918718) and the Sevilleta LTER Program. KAK acknowledges support from NSF (DEB-0315686, DBI-0420965, DBI-0521018) and the Michigan Sea Grant College Program (NA76RG0133) under NOAA. CRK acknowledges support from a DOE BER Science Focus Area grant. MEL and RLS acknowledge support from DOE BER Grant number DE-SC0008088. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

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Authors and Affiliations

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

    Robert L. Sinsabaugh, Marcy E. Litvak, Noelle G. Martinez & Daniel D. Warnock

  2. Southwest Biological Science Center, U.S. Geological Survey, Moab, UT, 84532, USA

    Jayne Belnap

  3. Cary Institute of Ecosystem Studies, Millbrook, NY, 12545, USA

    Stuart G. Findlay

  4. Watershed Sciences Department, Utah State University, Logan, UT, 84322, USA

    Jennifer J. Follstad Shah

  5. National Health and Environmental Effects Laboratory, Mid-Continent Ecology Division, Office of Research and Development, U.S. Environmental Protection Agency, Duluth, MN, 55804, USA

    Brian H. Hill

  6. Department of Biological Sciences, University of Southern Mississippi, Hattiesburg, MS, 39406, USA

    Kevin A. Kuehn

  7. Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, USA

    Cheryl R. Kuske

  8. Department of Environmental Science, University of Toledo, Toledo, OH, 43606, USA

    Daryl L. Moorhead

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  1. Robert L. Sinsabaugh
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Correspondence to Robert L. Sinsabaugh.

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Sinsabaugh, R.L., Belnap, J., Findlay, S.G. et al. Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121, 287–304 (2014). https://doi.org/10.1007/s10533-014-0030-y

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