Virus-associated organosulfur metabolism in human and environmental systems

• Published in: Cell reports (Cambridge) Vol. 36; no. 5; p. 109471
• Main Authors: Kieft, Kristopher, Breister, Adam M., Huss, Phil, Linz, Alexandra M., Zanetakos, Elizabeth, Zhou, Zhichao, Rahlff, Janina, Esser, Sarah P., Probst, Alexander J., Raman, Srivatsan, Roux, Simon, Anantharaman, Karthik
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 03.08.2021; Elsevier
• Subjects: auxiliary metabolism; bacteriophages; cysteine; Environment; Gastrointestinal Microbiome; Genes, Viral; Genetic Variation; Genomics; human microbiome; Humans; Metabolic Networks and Pathways - genetics; Microbiology; Microbiota; Mikrobiologi; Organic Chemicals - metabolism; organic sulfur; Phylogeny; Recombination, Genetic - genetics; sulfide; Sulfides - metabolism; Sulfur - metabolism; viruses; Viruses - genetics; Viruses - metabolism; viruses; human microbiome; cysteine; bacteriophages; auxiliary metabolism; sulfide; organic sulfur
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2021.109471

Viruses 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. Although 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, whereas others manipulate organosulfur compounds and may influence sulfide production. We show that viral metabolic genes encode key enzymatic domains, are translated into protein, and are maintained after recombination, and sulfide provides a fitness advantage to viruses. Our results reveal viruses as drivers of organosulfur metabolism with important implications for human and environmental health. [Display omitted] •Thousands of diverse viruses encode genes that manipulate organic sulfur metabolism•Infection in the presence of sulfide increases bacteriophage production•Engineered phage T7 retains cysteine synthase (cysK) over multiple generations•These viruses can influence human gut dysbiosis, microbiomes, and biogeochemistry Kieft et al. identify thousands of viruses that encode genes for organosulfur metabolism. They provide evidence for potential benefits of these genes to viruses, namely the role of organosulfur-derived hydrogen sulfide in increasing viral fitness. Their results have implications in exacerbation of human gut dysbiosis and global biogeochemical sulfur cycling.