Isolation and characterization of a roseophage representing a novel genus in the N4-like Rhodovirinae subfamily distributed in estuarine waters.

Abstract

Background: Roseobacteraceae, often referred to as the marine roseobacter clade (MRC), are pivotal constituents of bacterial communities in coastal and pelagic marine environments. During the past two decades, 75 roseophages that infect various Roseobacteraceae lineages have been isolated. The N4-like roseophage clade, which encompasses 15 members, represents the largest clade among these roseophages. N4-like phages form a monophyletic group, classified as family Schitoviridae. And all N4-like roseophages form a unique clade within Schitoviridae and has been classified as the Rhodovirinae subfamily.

Results: In this study, we isolated a novel roseophage, vB_DshP-R7L, that infects Dinoroseobacter shibae DFL12 from Xiamen Bay in the East China Sea. Conserved genes of Schitoviridae have been identified in the genome of vB_DshP-R7L, and following phylogenetic analysis suggests that the newly isolated phage is a member of the Rhodovirinae subfamily and represents the sole member of a novel genus, Gonggongvirus. The genome of vB_DshP-R7L harbors six auxiliary metabolic genes (AMGs), most of which potentially enhance DNA de novo synthesis. Additionally, a gene encoding ribosomal protein was identified. Comparative genomic analysis of AMG content among Rhodovirinae indicates a distinct evolutionary history characterized by independent ancient horizontal gene transfer events. Read-mapping analysis reveals the prevalence of vB_DshP-R7L and other Rhodovirinae roseophages in estuarine waters.

Conclusions: Our work illustrates the genomic features of a novel roseophage clade among the subfamily Rhodovirinae. The AMG content of vB_DshP-R7L is under severe purification selection, which reveals their possible ecological importance. We also demonstrated that vB_DshP-R7L and other Rhodovirinae roseophages are only detected in estuaries. Our isolation and characterization of this novel phage expands the understanding of the phylogeny, gene transfer history, and biogeography of Rhodovirinae infecting marine Roseobacteraceae.