Microbially Driven Physicochemical Destabilization in Organic Matter Turnover

Abstract

Abstract The persistence of organic matter has long been attributed to the intrinsic recalcitrance of complex biopolymers and the constraints of enzymatic degradation. However, across both marine and terrestrial ecosystems, structurally complex polymers such as chitin, cellulose, and lignin exhibit unexpectedly rapid turnover. This discrepancy reveals a mismatch between molecular-scale stability and ecosystem-scale carbon fluxes. Here, a new perspective, Microbial Physicochemical Priming (MPCP), is proposed to reconcile this paradox. MPCP is defined as the metabolism-driven physicochemical modification of the microenvironment that enhances the accessibility of complex organic matter to enzymatic depolymerization. Through the production of reactive intermediates, including reduced sulfur species, ferrous iron, reactive nitrogen species, and reactive oxygen species, microbial communities generate steep physicochemical gradients at submillimeter scales. These gradients induce physicochemical destabilization of polymer structures, increasing accessibility for subsequent enzymatic attack. MPCP posits that microbial metabolism actively engineers microscale physicochemical environments that precede or accompany and facilitate enzymatic hydrolysis. The metabolism-driven priming provides a bridge between microscale microbial activity and macroscale carbon cycling. Incorporating MPCP into biogeochemical models offers a pathway to resolve longstanding discrepancies in organic matter turnover and substantially improve predictions of carbon–climate feedbacks under environmental change.