Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming

Abstract

Most current models of soil C dynamics predict that climate warming will accelerate soil C mineralization, resulting in a long-term CO release and positive feedback to global warming. However, ecosystem warming experiments show that CO loss from warmed soils declines to control levels within a few years. Here, we explore the temperature dependence of enzymatic conversion of polymerized soil organic C (SOC) into assimilable compounds, which is presumed the rate-limiting step of SOC mineralization. Combining literature review, modelling and enzyme assays, we studied the effect of temperature on activity of enzymes considering their thermal inactivation and catalytic activity. We defined the catalytic power of enzymes (E ) as the cumulative amount of degraded substrate by one unit of enzyme until its complete inactivation. We show a universal pattern of enzyme's thermodynamic properties: activation energy of catalytic activity (EA ) < activation energy of thermal inactivation (EA ). By investing in stable enzymes (high EA ) having high catalytic activity (low EA ), microorganisms may maximize the E of their enzymes. The counterpart of such EAs' hierarchical pattern is the higher relative temperature sensitivity of enzyme inactivation than catalysis, resulting in a reduction in E under warming. Our findings could explain the decrease with temperature in soil enzyme pools, microbial biomass (MB) and carbon use efficiency (CUE) reported in some warming experiments and studies monitoring the seasonal variation in soil enzymes. They also suggest that a decrease in soil enzyme pools due to their faster inactivation under warming contributes to the observed attenuation of warming effect on soil C mineralization. This testable theory predicts that the ultimate response of SOC degradation to warming can be positive or negative depending on the relative temperature response of E and microbial production of enzymes.

Effects of <i>Solidago canadensis</i> Invasion and Climate Warming on Soil Net N Mineralization

“…However, the lower NNmin at warming than at the ambient was in agreement with the results of the earlier findings showing that both net and gross nitrification rates declined with increasing temperature from 15 to 20ºC [58]. These negative responses in NNmin to warming may be caused by the limited availability of soluble organic C in their soils [57], and the catalytic power of enzyme decreases with warming may also be a necessary reason [59]. The ANmin decreases with increasing soil temperature were also observed in [49], and were attributed to the lack of positive response in ammonification to increasing temperature to the accelerated immobilization of NH4 + -N by microbes [49,60].…”

Microbial growth and carbon use efficiency show seasonal responses in a multifactorial climate change experiment

“…This reversal effect was irrespective of atmospheric CO 2 concentration. The negative response of microbial activity to warming in July suggests that other environmental factors might have masked the inherent temperature sensitivity of microbial activity, as previously proposed 44,51 . Particularly, lower soil moisture might have been the leading cause of decreased biomass-specific growth and respiration and might have dampened the positive temperature response.…”

“…Field studies investigating climate change effects on microbial growth and CUE are scarce and have mostly focused on effects of warming. Studies on the response of microbial CUE to warming reported contradictory findings: some authors reported no effects of warming on microbial CUE 39,40 , while others observed reduced CUE [5][6][7]34,[41][42][43][44][45] , or increased microbial CUE 12 . However, these studies used a range of different approaches to estimate CUE 5 , which may not allow direct comparisons 6,8,46 .…”

Climate warming alters subsoil but not topsoil carbon dynamics in alpine grassland

“…This may be linked to several factors. First, underdegraded lignin in the subsoil (indicated by lignin Ad/Al ratios) may be more susceptible to degradation in the warmed soils with an extended period of microbial activity (Lin et al, ) and a potentially increased size of enzyme pools (Alvarez et al, ), highlighting the vulnerability of relatively fresh lignin partially “cryo‐locked” in the deep horizons of alpine soils. Second, microbial degradation of millennia‐old SOC was found to be fueled by increased inputs of labile carbon via root penetration to the deep layers of a temperate grassland (Shahzad et al, ).…”