Viral conversations with sulfur: Metabolic and biogeochemical implications of phage infections

Abstract:

Sulfur metabolism plays a critical role in the transformation of organic carbon compounds and nutrients in diverse environments. Viruses that infect microbes are the most abundant biological entities in most ecosystems. By infecting and lysing microbial populations, bacteriophages can affect microbial community composition and function which can directly impact nutrient cycles. Our current knowledge of ecology and biogeochemical cycling associated with this key element is primarily based on studies of microorganisms that overlook viruses. We used a combination of data-science driven and experimental approaches to uncover viral diversity and their impacts on metabolism associated with inorganic and organic sulfur transformations. Genomic and evolutionary analyses suggested that metabolic genes identified on viruses were under purifying selection, irrespective of the pathways they contribute to, the environments from which they were recovered, or the hosts that the viruses are associated with. Transcriptomic, qPCR, and proteomic analyses on a model host-phage system suggested that phage genes for sulfur metabolism were highly active during infection. Finally, creation of transgenic phages with genes for sulfur metabolism suggest they could complement host metabolism, and also outcompete wild type viruses hinting at the significant advantages provided by sulfur AMGs. Overall, our results provide motivation for integration of viruses and their impacts on metabolism into next-generation metabolic, ecosystem, and biogeochemical models.