Novel phage infecting the Roseobacter CHUG lineage reveals a diverse and globally distributed phage family

Abstract

Bacteriophages play an essential role in shaping the diversity and metabolism of bacterial communities. Marine Roseobacter group is an abundant heterotrophic bacterial group that is involved in many major element cycles, especially carbon and sulfur. Members of the Roseobacter CHUG (Clade Hidden and Underappreciated Globally) lineage are globally distributed and are activated in pelagic marine environments. In this study, we isolated and characterized a phage, CRP-810, that infects the CHUG strain FZCC0198. The genome of CRP-810 was dissimilar to those of other known phages. Additionally, 251 uncultured viral genomes (UViGs) closely related to CRP-810 were obtained from the uncultivated marine viral contig databases. Comparative genomic and phylogenetic analyses revealed that CRP-810 and these related UViGs exhibited conserved genome synteny, representing a new phage family with at least eight subgroups. Most of the CRP-810-type phages contain an integrase gene, and CRP-810 can be integrated into the host genome. Further analysis revealed that three CRP-810-type members were prophages found in the genomes of marine SAR11, Poseidonocella , and Sphingomonadaceae . Finally, viromic read-mapping analysis showed that CRP-810-type phages were globally distributed and displayed distinct biogeographic patterns related to temperature and latitude. Many members with a lower G + C content were mainly distributed in the trade station, whereas members with a higher G + C content were mainly distributed in polar and westerlies station, indicating that the niche differentiation of phages was subject to host adaptation. Collectively, these findings identify a novel phage family and expand our understanding of phylogenetic diversity, evolution, and biogeography of marine phages. IMPORTANCE The Roseobacter CHUG lineage, affiliated with the Pelagic Roseobacter Cluster (PRC), is widely distributed in the global oceans and is active in oligotrophic seawater. However, knowledge of the bacteriophages that infect CHUG members is limited. In this study, a CHUG phage, CRP-810, that infects the CHUG strain FZCC0198, was isolated and shown to have a novel genomic architecture. In addition, 251 uncultured viral genomes closely related to CRP-810 were recovered and included in the analyses. Phylogenomic analyses revealed that the CRP-810-type phages represent a new phage family containing at least eight genus-level subgroups. Members of this family were predicted to infect various marine bacteria. We also demonstrated that the CRP-810-type phages are widely distributed in global oceans and display distinct biogeographic patterns related to latitude. Collectively, this study provides important insights into the genomic organization, diversity, and ecology of a novel phage family that infect ecologically important bacteria in the global ocean.