Novel roseophages provide insights into a genetically and ecologically diverse phage family

Roseobacters are prevalent in marine environments and play a crucial role in global carbon and sulphur cycles. Although many roseophages that infect roseobacters have been characterized, those infecting members of the ecologically dominant pelagic Roseobacter cluster (PRC) remain largely unexplored due to the challenges of culturing these organisms. In this study, we isolated 7 phylogenetically related roseophages from 3 PRC lineages and retrieved 279 uncultured viral genomes (UViGs) related to these roseophages from marine environmental viral databases. Comparative genomic and phylogenetic analyses revealed that these roseophages and their related UViGs form a novel family-level phage group (designated the CRP-822-type group) comprising at least five subgroups. These subgroups display distinct genomic features in terms of G+C content, amino acid usage and codon usage, suggesting host-range specialization. Host prediction suggests that subgroup V with low G+C content may infect the SAR86 clade, while the high G+C subgroup IV likely infects the high G+C KI89A clade. Finally, viromic read-mapping analyses revealed that CRP-822-type phages are widely distributed across the global ocean and are adapted to diverse marine environments. All members of subgroup IV were more abundant in trade, westerlies and coastal regions with high temperatures. The other four subgroups exhibited more divergent biogeographic patterns, with some members more abundant in trade and westerlies ocean regions, whereas others dominated in polar or estuarine regions. Collectively, this study elucidates the genetic diversity and ecology of a previously unrecognized marine phage group that infects PRC roseobacters and other important marine bacteria.