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Hyperthermophilic composting (hTC) is a promising technique for solid waste treatment due to its distinctive microbiomes. However, the assembly process of the hTC microbial community remains unclear. We investigated the assembly process of hTC and explored the underlying drivers influencing community assembly in this work by employing conventional thermophilic composting (cTC) as a comparison group. Our results showed that the two composting treatments have different community assembly processes. Especially for the initial and thermophilic phases, hTC is affected by homogeneous dispersal (48%) and homogeneous selection (44%), respectively, while cTC is controlled by undominant (38%) and homogeneous selection (92%), respectively. Furthermore, random forest models and network results suggested that different factors govern the community assembly in these two composting methods. Specifically, the hTC community increases the stability of the thermophilic community via enhancing the interactions of low-abundance taxa with other operational taxonomic units (OTUs) in community assembly. Our results suggested that the distinctive nature of hTC community assembly may be responsible for its adaptation to extreme environments.

Publisher Copyright: © 2023, The Author(s). While decomposition of organic matter by bacteria plays a major role in nutrient cycling in terrestrial ecosystems, the significance of viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study the significance of mesophilic and thermophilic bacteria and their viruses on nutrient cycling during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics and activity are tightly coupled, where viruses specific to mesophilic and thermophilic bacteria track their host densities, triggering microbial community succession via top-down control during HTC. Moreover, viruses specific to mesophilic bacteria encoded and expressed several auxiliary metabolic genes (AMGs) linked to carbon cycling, impacting nutrient turnover alongside bacteria. Nutrient turnover correlated positively with virus–host ratio, indicative of a positive relationship between ecosystem functioning, viral abundances, and viral activity. These effects were predominantly driven by DNA viruses as most detected RNA viruses were associated with eukaryotes and not associated with nutrient cycling during the thermophilic phase of composting. Our findings suggest that DNA viruses could drive nutrient cycling during HTC by recycling bacterial biomass through cell lysis and by expressing key AMGs. Viruses could hence potentially be used as indicators of microbial ecosystem functioning to optimize productivity of biotechnological and agricultural systems.

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.

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.