Insights into Extracellular Respiration Interfaces: Linking Molecular Redox Sites to Humic-Reducing Microorganisms in Biowaste Compost

Composting forms a vital bridge between organic waste and agricultural soil. Microbial-mediated extracellular electron transfer (EET) during composting governs material and energy flows, determines compost functionality, and ultimately influences soil redox cycling. However, elucidating the EET chain from humic-reducing microorganisms (HRMs) to molecular redox sites remains a significant challenge. Here, we integrated molecular metacommunity ecology with a theoretical molecular model to probe HRM-mediated EET at microinterfaces, correlating redox sites, intermolecular interactions, and bulk-surface molecular properties. Thirty-five models corresponding to 88 HRMs were constructed, correlating electron-accepting/-donating capacity (EAC/EDC)-related molecules with HRMs. The EET chain of electron donors, HRMs, and redox sites was established based on 3D imaging snapshots of condensed molecules. In Composts I–III, 10–21, and 6–12 HRMs preferentially targeted lignin-derived polyphenols and aliphatic/protein substrates, respectively. Additionally, Luteimonas and Paenibacillus promoted diverse degradation pathways. For back-end electron acceptors, HRMs showed selective utilization of Ar–SH, Ar–COO–, and quinone from EAC-related molecules, with preferences varying by HRMs and composts. This process is significantly influenced by intermolecular interactions (H-bond, salt bridge, aromatic-H, π-stacking, and cation−π) and molecular aggregation behavior. This work offers a novel theoretical foundation for regulating the redox process during composting, enhancing resource conversion efficiency, and guiding the development of high-function compost products.