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.