Abstract
ABSTRACTViruses are the most abundant living entities in marine ecosystems, playing critical roles in altering the structure and function of microbial communities and driving ocean biogeochemistry. Phages that infect Roseobacter clade-affiliated (RCA) cluster strains are an important component of marine viral communities. Here, we characterize the genome sequences of two new RCA phages, CRP-9 and CRP-13, which infect RCA strain FZCC0023. Genomic analysis reveals that CRP-9 and CRP-13 represent a novel evolutionary lineage of marine phages. They both have a DNA replication module most similar to those in Cobavirus group phages. In contrast, their morphogenesis and packaging modules are distinct from those in cobaviruses but homologous to those in HMO-2011-type phages. The genomic architecture of CRP-9 and CRP-13 suggests a genomic recombination event between distinct phage groups. Metagenomic data sets were examined for metagenome-assembled viral genomes (MAVGs) with similar recombinant genome architectures. Fifteen CRP-9-type MAVGs were identified from marine viromes. Additionally, 158 MAVGs were identified containing HMO-2011-type morphogenesis and packaging modules with other types of DNA replication genes, providing more evidence that recombination between different phage groups is a major driver of phage evolution. Altogether, this study significantly expands the understanding of diversity and evolution of marine roseophages. Meanwhile, the analysis of these novel RCA phages and MAVGs highlights the critical role of recombination in shaping phage diversity. These phage sequences are valuable resources for inferring the evolutionary connection of distinct phage groups.IMPORTANCE Diversity and evolution of phages that infect the relatively slow-growing but dominant Roseobacter lineages are largely unknown. In this study, RCA phages CRP-9 and CRP-13 have been isolated on a Roseobacter RCA strain and shown to have a unique genomic architecture, which appears to be the result of a recombination event. CRP-9 and CRP-13 have a DNA replication module most similar to those in Cobavirus group phages and morphogenesis and packaging modules most similar to those in HMO-2011-type phages. HMO-2011-type morphogenesis and packaging modules are found in combination with distinct types of DNA replication genes, suggesting compatibility with various DNA replication modules. Altogether, this study contributes toward a better understanding of marine viral diversity and evolution.
Highlights
IMPORTANCE Diversity and evolution of phages that infect the relatively slow-growing but dominant Roseobacter lineages are largely unknown
MicrobiolSpectrum.asm.org 1 they have successfully obtained a large amount of genetic information of double-stranded DNA metagenome-assembled viral genomes (MAVGs) [5,6,7,8]
Despite the enormous number of available viral genomes retrieved from metagenomic studies, the majority of MAVGs have limited similarity to phage isolates, and most open reading frames (ORFs) remained unannotated
Summary
IMPORTANCE Diversity and evolution of phages that infect the relatively slow-growing but dominant Roseobacter lineages are largely unknown. RCA phages CRP-9 and CRP-13 have been isolated on a Roseobacter RCA strain and shown to have a unique genomic architecture, which appears to be the result of a recombination event. Current knowledge of the genetic diversity of phages suggests that genomic evolution of bacteriophages is mainly driven by extensive lateral gene transfer via genetic recombination and fast mutation [12,13,14]. Due to difficulties in host cultivation, researchers have only begun to explore the diversity and ecology of phages infecting dominant Roseobacter lineages. In 2019, Zhang et al first reported phages infecting RCA strains [30] These RCA phages are genetically and evolutionarily diverse, belonging to four distinct phage groups [30]. Our results expand the understanding of the roseophages and have broader implications for understanding the evolution of marine phages
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