Synergy between reactive manganese species and enzymes drives litter decomposition hotspots

Abstract

Abstract Oxidative decomposition of plant litter is a central control on carbon storage and productivity in terrestrial ecosystems. Although this process is commonly assumed to be greatest under oxic conditions, recent findings highlight redox-sensitive metals and enzymes as potent, but poorly understood, mediators. Using controlled soil reactors, we show that stimulating microbial production of reactive manganese(III) at oxic–anoxic interfaces simultaneously increased the expression of diverse litter-decomposing enzymes; together, these metal and enzyme catalysts acted synergistically to accelerate litter decomposition. This 29% increase in decomposition was best predicted by multi-fold increases in the expression of putative Mn(III)-forming and litter-degrading enzymes at the interface, rather than by patterns in strictly oxic or anoxic zones. These results provide evidence to the growing body of research challenging the assumption that oxidative decomposition is maximized under fully oxic conditions. Instead, they reveal a tight interplay among oxygen supply, reactive metal regeneration, and enzyme activity that renders oxic–anoxic interfaces hotspots of litter decomposition in soils.