Large mammalian herbivores influence the deployment of microbial extracellular enzymes to control soil carbon cycling

Abstract

Large mammalian grazers have regulated biogeochemical cycles across 40% of the Earth’s terrestrial surface for millennia. While grazer effects on organic matter entering the soil are becoming clear, their effect on the downstream microbial foraging through extracellular-enzymes (EE), which link processes at the cellular level to ecosystem-level flow of matter remain less clear. We assessed how large mammalian grazers influence microbial foraging in soil using two lines of evidence. First, utilising a 14-year-old long-term grazer-exclusion experiment in the Trans-Himalayan ecosystem, we find that activities of seven enzymes peak at different months during the growing-season in an asynchronous manner. Microbial deployment of enzymes responded to grazer-exclusion by shifting from nitrogen (N)-acquisition in spring to carbon (C)- and phosphorus (P)-acquisition in summer and autumn. Grazer exclusion increased peroxidase activity by 124.7% and β-glucosidase by 16.7%. About half of the variation in enzyme portfolios was explained by seasonal differences in grazer effects. Grazer-exclusion increased the variability in the enzyme portfolio, requiring the microbes to forage across a larger portion of the functional space. Structural equation models suggested that grazer-exclusion worsens the quality of biomass input to soil due to an 18% increase in acid-unhydrolysable recalcitrant C. As seen in other ecosystems, this decline in substrate quality raises microbial deployment of generic depolymerizers relative to the specialized enzymes which release assimilable end-products. As greater investment in generic depolymerizing enzymes may reduce microbial carbon use efficiency, it can affect the C cycle. Second, laboratory incubations supported that soil enzymes are indeed inducible/repressible in response to experimental manipulation of biomass quality. Microbial responses appear predictable and generalisable across spatial scales, from laboratory-incubations to whole ecosystems. Hence, fostering microbial functions can enhance the scope and efficacy of rewilding and restoration for natural climate solutions.