Extracellular enzyme kinetics scale with resource availability

Robert L. Sinsabaugh, Jayne Belnap, Stuart G. Findlay, Jennifer J.Follstad Shah, Brian H. Hill, Kevin A. Kuehn, Cheryl R. Kuske, Marcy E. Litvak, Noelle G. Martinez, Daryl L. Moorhead, Daniel D. Warnock

Research output: Contribution to journalArticlepeer-review

147 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)287-304
Number of pages18
JournalBiogeochemistry
Volume121
Issue number2
DOIs
StatePublished - Oct 2 2014
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2014, Springer International Publishing Switzerland.

Keywords

  • Ecological stoichiometry
  • Enzyme kinetics
  • Extracellular enzymes
  • Microbial community
  • Microbial metabolism

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