Virus-associated organosulfur metabolism in human and environmental systems

Abstract

SummaryViruses influence the fate of nutrients and human health by killing microorganisms and altering metabolic processes. Organosulfur metabolism and biologically-derived hydrogen sulfide play dynamic roles in manifestation of diseases, infrastructure degradation, and essential biological processes. While microbial organosulfur metabolism is well-studied, the role of viruses in organosulfur metabolism is unknown. Here we report the discovery of 39 gene families involved in organosulfur metabolism encoded by 3,749 viruses from diverse ecosystems, including human microbiomes. The viruses infect organisms from all three domains of life. Six gene families encode for enzymes that degrade organosulfur compounds into sulfide, while others manipulate organosulfur compounds and may influence sulfide production. We show that viral metabolic genes encode key enzymatic domains, are translated into protein, are maintained after recombination, and that sulfide provides a fitness advantage to viruses. Our results reveal viruses as drivers of organosulfur metabolism with important implications for human and environmental health.

Optimization and Ev a Luation of Viral Metagenomic Amplification and Sequencing Methods Toward a Genome -le Vel Resolution of the Human Fecal DNA Virome

“…Interestingly, we found that a large proportion of viral AMGs was involved in sulfur metabolism, in agreement with recent reports that the viruses are widely participants in both organic and inorganic sulfur metabolism in human gut [34,35]. The sul de provides a tness advantage to viruses and viruses also are drivers of organosulfur metabolism with important implications for human health [34]. Since most VLPs were bacteriophages within bacterial hosts, peptidoglycan metabolismrelated enzymes were frequently encoded by the viruses which are consistent with our viral AMGs results (up to 11.4%), such as peptidoglycan DL-endopeptidase function as both cell wall hydrolases and poly-γglutamic acid hydrolases [36], which may facilitate the interaction with the bacterial host.…”

“…Few eukaryotic viruses may be related to the ltering operation in the virus enrichment process. Interestingly, we found that a large proportion of viral AMGs was involved in sulfur metabolism, in agreement with recent reports that the viruses are widely participants in both organic and inorganic sulfur metabolism in human gut [34,35]. The sul de provides a tness advantage to viruses and viruses also are drivers of organosulfur metabolism with important implications for human health [34].…”

“…Strikingly, 22.7% of viral AMGs were involved in sulfur metabolism (Fig. 4b), in agreement with recent reports that the viruses are widely participants in both organic and inorganic sulfur metabolism in human gut [34,35]. The proteins involved in the destructive metabolism of peptidoglycan (an important struct of bacterial cell walls) were frequently encoded by the viruses (consisting of 11.4% AMGs), such as peptidoglycan DL-endopeptidase function as both cell wall hydrolases and poly-γ-glutamic acid hydrolases [36], which would facilitate infection and tness of bacterial host by such viruses.…”

Gut virome dysbiosis following focal cerebral ischemia in mice

“…30 Furthermore, AMGs of viruses are known to be transcribed during infection and involved in viral replication, fitness, and host interactions by direct involvement in the host metabolism. 33 Identifying AMGs involved in metabolic pathways that can influence inflammatory responses, such as sulfur metabolism and sulfide production, may provide insights into the impacts of virome changes on stroke outcomes. 33 The proportion of virulent phages increases in patients with digestive or respiratory system diseases compared to healthy individuals.…”

Environmental viromes reveal global virosphere of deep-sea RNA viruses

“…Given the crucial roles of sulfur metabolism in deep-sea ecosystems 4,19 , we analyzed the type and abundance of virus-encoded genes that mediate sulfur metabolism in four deep-sea habitats. A total of 10 viral genes were identified that are involved in assimilatory sulfate reduction and thiosulfate oxidation, the most important processes in sulfur metabolism [20][21][22] . The relative abundance of these 10 genes was significantly higher in hydrothermal vents compared to the other deep-sea habitats (Fig 4E ), which is consistent with the high sulfur concentration in hydrothermal vent ecosystems.…”