Aquatic Biofilm as a Hotspot for Manganese Oxidation Enabled by Microbial Extracellular Matrix-Mediated Dual-Pathway Electron Transfer
Mu-Cen Yao, Qi Huang, Hong-Xuan Xie, Xin Zhang, Guo‐Ping Sheng
Abstract
Manganese(II) oxidation governs the geochemical cycles of numerous elements owing to the exceptional oxidation and adsorption properties of resultant manganese oxide minerals. This process is predominantly thought to be driven by microorganisms using cellular oxidoreductases. Herein, we uncovered a new pathway for microbial manganese(II) oxidation mediated by a biofilm extracellular matrix, i.e., extracellular polymeric substances (EPS) secreted by microorganisms. Owing to abundant EPS, the biofilm emerged as a hotspot for manganese(II) oxidation in a sunlit aquatic system, and its ability to oxidize manganese(II) was 2.9 times higher than that of free microorganisms when normalized by the cell number. Both oxidoreductases such as NAD(P)H-oxidizing enzymes and nonenzymatic redox components like flavins and quinones in the EPS mediated electron transfer from intracellular NADPH to oxygen to produce superoxide. Additionally, quinones within the EPS under light irradiation mediated electron transfer from reducing moieties (e.g., thiols and phenols) in the extracellular matrix to oxygen to generate superoxide. As a result, EPS boosted manganese(II) oxidation via superoxide generated by these two electron transfer pathways. This biofilm-driven rapid manganese(II) oxidation process was found to be prevalent across diverse sunlit aquatic environments. This study expands the framework of microbe-driven cycling of manganese as well as other elements in nature.