Multiple Roles of Extracellular Vesicles in Promoting Microbial-Driven Manganese Reduction

Microbial-driven manganese (Mn) reduction influences the geochemical cycling of Mn and the environmental fate of various organic and inorganic substances. Extracellular vesicles (EVs) are known to impact microbial metabolic activities, but their specific role in Mn reduction remains arcane. Here, we explored the potential involvement of environmental EVs in this process through metagenomic analysis and validated their function using representative functional strains. There are 8.05 and 12.89% of EVs originating from electroactive microorganisms in soil and wastewater, respectively. The addition of EVs increases the birnessite reduction rate of <i>Shewanella oneidensis</i> MR-1 from 2.31 μmol/(L·h) to 20.86 μmol/(L·h). Microbial physiological assays and in situ electrochemical analyses revealed that EVs enhanced cellular metabolism, promoted biofilm formation, and facilitated extracellular electron transfer (EET). The presence of diverse redox enzymes and metabolites in EVs contributed to more efficient substrate utilization and energy conservation, which promoted biomass accumulation and increased substrate consumption by 45.33%. The inner and outer membrane <i>c</i>-type cytochromes, along with flavins contained in the EVs, are essential for promoting microbial EET. These findings highlight the multifaceted role of EVs in microbial-driven Mn reduction, which might also participate in other element cycles in the same way.