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

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.