Redox Transitions as Microbial Hotspots of Manganese-Mediated Organic MatterDegradation

<p>Oxic-anoxic interfaces serve as hotspots of organic matter decomposition, regulating soil and sediment carbon storage and nutrient cycling. Oxic-anoxic interfaces present along redox gradients, which are ubiquitous in soil and sediment environments, also serve as hotspots of reactive Mn(III) formation and Mn(III)-mediated organic matter degradation. Reactive manganese represents an important control on organic matter degradation in soil and sediment environments, impacting both greenhouse gas emissions and carbon storage. Mn(III) formation at redox interfaces depend not just on soil redox conditions, but also on microbially-mediated Mn redox cycling across the redox gradient. However, the extent to which microbially-mediated Mn(III) formation and subsequently Mn(III)-driven organic matter oxidation depends on Mn availability remains largely unknown. In this study, we quantified how variations in Mn bioavailability affects the microbial pathway and rates of Mn(III)-driven organic matter degradation across redox interfaces. To achieve this, we established redox gradients within forest soils using diffusion reactors and varied Mn availability in the anoxic zone, thereby controlling Mn(II) mobilization to the oxic-anoxic interface. We quantified changes in microbial activity and function in relation to Mn(III) formation and organic matter degradation across the redox gradient over a 12-week incubation period. Metatranscriptomics revealed Mn(II)-oxidizing enzymes responded strongly to Mn bioavailability at the redox interface, while qPCR showed that shifts in microbial community composition coincided with Mn(III) formation. Wet-chemical extractions combined with Mn XANES indicated that Mn(III) formation at the redox interface peaked after 4 weeks of incubation and was most pronounced with increasing M availability. Bioassays, combined with soil respiration measurements and carbon NEXAFS indicated organic matter degradation increased with increasing Mn availability, coinciding with the formation of Mn(III) at redox interfaces. Combined, our results show that redox gradients and oxic-anoxic interfaces serve as hotspots for Mn(III) formation and subsequent organic matter degradation and are driven by enhanced Mn availability. Our work highlights the critical role of Mn redox cycling within microbial hotspots may have in regulating carbon dynamics in terrestrial environments. </p>