Temperature sensitivities of extracellular enzyme V_max and K_m across thermal environments

Abstract

The magnitude and direction of carbon cycle feedbacks under climate warming remain uncertain due to insufficient knowledge about the temperature sensitivities of soil microbial processes. Enzymatic rates could increase at higher temperatures, but this response could change over time if soil microbes adapt to warming. We used the Arrhenius relationship, biochemical transition state theory, and thermal physiology theory to predict the responses of extracellular enzyme V and K to temperature. Based on these concepts, we hypothesized that V and K would correlate positively with each other and show positive temperature sensitivities. For enzymes from warmer environments, we expected to find lower V , K , and K temperature sensitivity but higher V temperature sensitivity. We tested these hypotheses with isolates of the filamentous fungus Neurospora discreta collected from around the globe and with decomposing leaf litter from a warming experiment in Alaskan boreal forest. For Neurospora extracellular enzymes, V Q ranged from 1.48 to 2.25, and K Q ranged from 0.71 to 2.80. In agreement with theory, V and K were positively correlated for some enzymes, and V declined under experimental warming in Alaskan litter. However, the temperature sensitivities of V and K did not vary as expected with warming. We also found no relationship between temperature sensitivity of V or K and mean annual temperature of the isolation site for Neurospora strains. Declining V in the Alaskan warming treatment implies a short-term negative feedback to climate change, but the Neurospora results suggest that climate-driven changes in plant inputs and soil properties are important controls on enzyme kinetics in the long term. Our empirical data on enzyme V , K , and temperature sensitivities should be useful for parameterizing existing biogeochemical models, but they reveal a need to develop new theory on thermal adaptation mechanisms.

Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient

“…). Overall, despite the result for phenol oxidase, the Q 10 of V max for the remaining six enzymes was not affected by warming (Figs and ), consistent with a recent global study showing an insensitivity of Q 10 of V max to temperature for the majority of enzymes (Allison et al ). These results indicate that the dominant effect of enzymatic responses to warming on soil C result from changes in V max , rather than the Q 10 of V max , whether reduced (by thermal compensation) or increased as shown here (Fig.…”

“…Temperature adaptation of enzyme function across natural temperature gradients has been associated with differences in the temperature sensitivity ( Q 10 response) of activity ( V max ), and with decreased Q 10 of V max at higher temperature ranges (Brzostek & Finzi ; Nottingham et al ), although there is also evidence for the insensitivity of Q 10 of V max for soil enzymes across natural temperature gradients (Allison et al ). This pattern of long‐term temperature response of enzyme activity was supported for only one out of seven measured enzymes (phenol oxidase) following the 5 years of temperature manipulation.…”

“…an 'enhancing' CUE response) (Wieder et al 2013). The underlying mechanisms for these CUE responses remain unclear, but might include physiological changes within species, shifts in microbial community composition (Oliverio et al 2017), or changes in the temperature sensitivity of enzyme activity (Wallenstein et al 2011;Allison et al 2018).…”

A Theory of Effective Microbial Substrate Affinity Parameters in Variably Saturated Soils and an Example Application to Aerobic Soil Heterotrophic Respiration

“…Monod () also fitted his model to obtain the glucose affinity parameter from a culture of Escherichia coli in a diluted solution of synthetic medium. Further, enzyme assays of potential soil enzyme activities and their substrate affinity parameters are conducted using microplates which hold well‐mixed solutions of substrates and soil samples (Allison et al, ; German et al, ; Loeppmann et al, ; Sihi et al, ; Zhang et al, ). Although petri dishes used for bacterial culture may contain agar gel, the kinetic parameters are still derived by assuming that substrate delivery is not diffusion limited (e.g., Koch, ).…”

Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in a warmer world

“…Variation in the temperature sensitivity of growth efficiency could be driven by differences in the rate-limiting step of central metabolic pathways (Dijkstra et al, 2011a), or in how well the proteins responsible for the extracellular processing and uptake of environmental nutrients are able to maintain activity as temperature increases (Allison et al, 2018;Alster et al, 2018). For instance, there is some evidence that bacteria benefit more than fungi from an increase in temperature, as their growth rate was observed to decrease less rapidly with temperature above its optimum than the fungal community's did .…”