Novel phage–host interactions and evolution as revealed by a cyanomyovirus isolated from an estuarine environment

Cyanophages are thought to affect the community structure, population dynamics, metabolic activity and evolution of picocyanobacteria and to impact the biogeochemical cycling in aquatic ecosystems. Here, we report an estuarine Synechococcus phage, S-CBWM1, which represents a novel viral lineage and exhibits interesting genetic features related to phage–host interactions and evolution. S-CBWM1 encapsidates four virion-associated proteins related to cellular metabolic regulation. Several novel auxiliary metabolic genes related to multidrug efflux, cell wall and capsule synthesis or modifications were also identified. In addition, the presence of the largest number of tRNA genes hitherto found in a phage genome may contribute to the translation efficiency of unique genes. These genomic and proteomic features of S-CBWM1 suggested phage–host interactions involved in adaptation to eutrophic estuarine environments. Phylogenetic and metagenomic analysis of the polγ gene in the S-CBWM1 genome provided new insights into the evolutionary path of mitochondrial DNA polymerase gamma. The S-CBWM1 psbA contains two group I introns, representing the first instance of multiple introns within psbA from phage. The isolation of S-CBWM1 reveals that estuarine ecosystems contain evolutionarily novel cyanophages that drive unique phage–host interactions.