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.

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The emergence of multidrug-resistant bacterial pathogens poses a serious global health threat. While patient infections by the opportunistic human pathogen Pseudoxanthomonas spp. have been increasingly reported worldwide, no phage associated with this bacterial genus has yet been isolated and reported. In this study, we isolated and characterized the novel phage PW916 to subsequently be used to lyse the multidrug-resistant Pseudoxanthomonas kaohsiungensi which was isolated from soil samples obtained from Chongqing, China. We studied the morphological features, thermal stability, pH stability, optimal multiplicity of infection, and genomic sequence of phage PW916. Transmission electron microscopy revealed the morphology of PW916 and indicated it to belong to the Siphoviridae family, with the morphological characteristics of a rounded head and a long noncontractile tail. The optimal multiplicity of infection of PW916 was 0.1. Moreover, PW916 was found to be stable under a wide range of temperatures (4–60 °C), pH (4–11) as well as treatment with 1% (v/w) chloroform. The genome of PW916 was determined to be a circular double-stranded structure with a length of 47,760 bp, containing 64 open reading frames that encoded functional and structural proteins, while no antibiotic resistance nor virulence factor genes were detected. The genomic sequencing and phylogenetic tree analysis showed that PW916 was a novel phage belonging to the Siphoviridae family that was closely related to the Stenotrophomonas phage. This is the first study to identify a novel phage infecting the multidrug-resistant P. kaohsiungensi and the findings provide insight into the potential application of PW916 in future phage therapies.

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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.