Microbial Community Restructuring Drives Metabolic Shifts to Enhance Humification in Hyperthermophilic Food Waste Composting

Conventional composting struggles with slow fermentation and low humification efficiency in managing global food waste. While hyperthermophilic composting (HTC, >80 °C) can enhance efficiency, the microbial and metabolic drivers of accelerated humification remain unknown. Multi-omics analysis revealed that microbial restructuring during the HTC cooling stage (30–80 °C) triggers metabolic reprogramming. Enriched thermophiles (e.g., Gordonia, Cryptosporangium, Limnochordia) redirect carbon flux toward anabolism via upregulated glycolysis/gluconeogenesis and aromatic amino acid biosynthesis, while suppressing the TCA cycle. This redirected carbon flux accelerated lignocellulose degradation (2.6–3.7-fold), boosted humic acid synthesis (by 50%), and increased the humification index (by 76%). Critically, it promoted the condensation of lignin-derived phenolics with amino acids and Maillard-mediated polymerization, increasing aromatic precursors by 161%. Structural equation modeling demonstrated a strong association between microbial restructuring and humic substance formation, explaining 96% of the total variance through metabolic regulation. These mechanistic insights enable the design of high-efficiency composting systems for simultaneous waste valorization and stable humic substance production.