Unexpected Myriad of Co-occurring Viral Strains and Species in One of the Most Abundant and Microdiverse Viruses on Earth

Viral genetic microdiversity drives adaptation, pathogenicity, and speciation and has critical consequences for the viral-host arms race occurring at the strain and species levels, which ultimately impact microbial community structure and biogeochemical cycles. Despite the fact that most efforts have focused on viral macrodiversity, little is known about the microdiversity of ecologically important viruses on Earth. Recently, single-virus genomics discovered the putatively most abundant ocean virus in temperate and tropical waters: the uncultured dsDNA virus vSAG 37-F6 infecting Pelagibacter, the most abundant marine bacteria. In this study, we report the cooccurrence of up to ≈1,500 different viral strains (>95% nucleotide identity) and ≈30 related species (80-95% nucleotide identity) in a single oceanic sample. Viral microdiversity was maintained over space and time, and most alleles were the result of synonymous mutations without any apparent adaptive benefits to cope with host translation codon bias and efficiency. Gene flow analysis used to delimitate species according to the biological species concept (BSC) revealed the impact of recombination in shaping vSAG 37-F6 virus and Pelagibacter speciation. Data demonstrated that this large viral microdiversity somehow mirrors the host species diversity since ≈50% of the 926 analyzed Pelagibacter genomes were found to belong to independent BSC species that do not significantly engage in gene flow with one another. The host range of this evolutionarily successful virus revealed that a single viral species can infect multiple Pelagibacter BSC species, indicating that this virus crosses not only formal BSC barriers but also biomes since viral ancestors are found in freshwater.