Keystone Genes Confer Superior Performance in Hyperthermophilic Composting

Abstract Background: Large amounts of organic solid wastes originating from anthropogenic activities have imposed enormous pressure on the environment and human health. Our previous studies showed that compared with conventional thermophilic composting (cTC), hyperthermophilic composting (hTC) exhibits superior performance in organic solid waste disposal by providing advantages such as improved composting temperature, nitrogen conservation (NC), nitrous oxide (N2O) mitigation and germination index (GI). However, it remains unclear how hTC communities drive improved performance. Here, we used GeoChip 5.0M coupled with high-throughput 16S rRNA gene sequencing data to investigate the variations in carbon (C)-degrading and nitrogen (N)-cycling genes and microbial communities and their linkages with selected performance indices (composting temperature, NC, N2O emission rate and GI) in hTC and cTC in factory-scale experiments, aiming to identify the keystone biotic drivers for the improved performance. Results: We showed that hTC significantly altered functional composition structures compared with those in cTC, which was driven by taxonomic shift in microbial communities. Specifically, hTC significantly increased the relative abundance of C-degrading genes and decreased the relative abundance of N-cycling genes during composting. These significantly shifted genes were the keystone genes dominating the improved performance of hTC, as indicated by a random forest model. Furthermore, network and partial least squares path modeling analysis suggested that the keystone genes continued to dominantly drive the improved performance after multiple biotic (community composition and other genes) drivers were simultaneously considering in hTC. Conclusions: Together, our study provides evidence that keystone genes potentially play a pivotal role in improving composting temperature, N2O mitigation, NC and GI in hTC and emphasizes the importance of understanding the variation in functions for targeted manipulation of composting practices.