Temperature Sensitivity as a Microbial Trait Using Parameters from Macromolecular Rate Theory

Charlotte J Alster; Peter Baas; Matthew D Wallenstein; Nels G Johnson; Joseph C von Fischer

doi:10.3389/fmicb.2016.01821

Temperature Sensitivity as a Microbial Trait Using Parameters from Macromolecular Rate Theory

Front Microbiol. 2016 Nov 17:7:1821. doi: 10.3389/fmicb.2016.01821. eCollection 2016.

Authors

Charlotte J Alster¹, Peter Baas², Matthew D Wallenstein³, Nels G Johnson⁴, Joseph C von Fischer¹

Affiliations

¹ Department of Biology, Colorado State University, Fort CollinsCO, USA; Graduate Degree Program in Ecology, Colorado State University, Fort CollinsCO, USA.
² Natural Resource Ecology Laboratory, Colorado State University, Fort Collins CO, USA.
³ Graduate Degree Program in Ecology, Colorado State University, Fort CollinsCO, USA; Natural Resource Ecology Laboratory, Colorado State University, Fort CollinsCO, USA; Department of Ecosystem Science and Sustainability, Colorado State University, Fort CollinsCO, USA.
⁴ National Institute for Mathematical and Biological Synthesis, University of Tennessee, Knoxville TN, USA.

Abstract

The activity of soil microbial extracellular enzymes is strongly controlled by temperature, yet the degree to which temperature sensitivity varies by microbe and enzyme type is unclear. Such information would allow soil microbial enzymes to be incorporated in a traits-based framework to improve prediction of ecosystem response to global change. If temperature sensitivity varies for specific soil enzymes, then determining the underlying causes of variation in temperature sensitivity of these enzymes will provide fundamental insights for predicting nutrient dynamics belowground. In this study, we characterized how both microbial taxonomic variation as well as substrate type affects temperature sensitivity. We measured β-glucosidase, leucine aminopeptidase, and phosphatase activities at six temperatures: 4, 11, 25, 35, 45, and 60°C, for seven different soil microbial isolates. To calculate temperature sensitivity, we employed two models, Arrhenius, which predicts an exponential increase in reaction rate with temperature, and Macromolecular Rate Theory (MMRT), which predicts rate to peak and then decline as temperature increases. We found MMRT provided a more accurate fit and allowed for more nuanced interpretation of temperature sensitivity in all of the enzyme × isolate combinations tested. Our results revealed that both the enzyme type and soil isolate type explain variation in parameters associated with temperature sensitivity. Because we found temperature sensitivity to be an inherent and variable property of an enzyme, we argue that it can be incorporated as a microbial functional trait, but only when using the MMRT definition of temperature sensitivity. We show that the Arrhenius metrics of temperature sensitivity are overly sensitive to test conditions, with activation energy changing depending on the temperature range it was calculated within. Thus, we propose the use of the MMRT definition of temperature sensitivity for accurate interpretation of temperature sensitivity of soil microbial enzymes.

Keywords: MMRT; Q10; activation energy; extracellular enzymes; macromolecular rate theory; microbial isolates; temperature optimum; trait-based ecology.