Abundances of keystone genes confer superior performance in hyperthermophilic composting

Abstract Large amounts of organic solid waste (OSW) originating from anthropogenic activities have imposed enormous pressure on the environment and human health. Hyperthermophilic composting (hTC) exhibits superior performance in OSW disposal by providing advantages such as improved composting temperature, nitrogen conservation (NC), nitrous oxide mitigation and germination index (GI) over conventional thermophilic composting (cTC). However, microbial communities have a central role in driving composting performance by mediating OSW component transformation, and it remains unclear how hTC communities drive improved performance. This study used GeoChip coupled with high-throughput sequencing data to investigate the variations in carbon (C)-degrading and nitrogen (N)-cycling genes and microbial communities and their linkages with performance indices in hTC and cTC, aiming to identify the keystone biotic drivers for the improved performance. The results indicated significant differences in the composition and structure profiles of the functional genes between the hTC and cTC treatments. 18 of 45 C-degrading genes exhibited significantly higher relative abundances during the hyperthermophilic phase in hTC (day 5) than in cTC. By comparison, 12 of 16 N-cycling genes showed significantly lower relative abundances in hTC than in cTC. These differences between hTC and cTC remained as the composting process proceeded but with a narrowed downward trend. These significantly shifted genes were the keystone genes dominating the improved performance of hTC, as indicated by a random forest model. Multiple statistical analyses suggested that the abundances of keystone genes continued to dominantly drive the improved performance after multiple biotic drivers were simultaneously considered in hTC. This study provides evidence that the abundance of keystone genes potentially plays a pivotal role in improving composting performance in hTC.