Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments

The SAR11 clade is one of the most abundant bacterioplankton groups in surface waters of most of the oceans and lakes. However, only 15 SAR11 phages have been isolated thus far, and only one of them belongs to the Myoviridae family (pelagimyophages). Here, we have analyzed 26 sequences of myophages that putatively infect the SAR11 clade. They have been retrieved by mining ca. 45 Gbp aquatic assembled cellular metagenomes and viromes. Most of the myophages were obtained from the cellular fraction (0.2 μm), indicating a bias against this type of virus in viromes. We have found the first myophages that putatively infect Candidatus Fonsibacter (freshwater SAR11) and another group putatively infecting bathypelagic SAR11 phylogroup Ic. The genomes have similar sizes and maintain overall synteny in spite of low average nucleotide identity values, revealing high similarity to marine cyanomyophages. Pelagimyophages recruited metagenomic reads widely from several locations but always much more from cellular metagenomes than from viromes, opposite to what happens with pelagipodophages. Comparing the genomes resulted in the identification of a hypervariable island that is related to host recognition. Interestingly, some genes in these islands could be related to host cell wall synthesis and coinfection avoidance. A cluster of curli-related proteins was widespread among the genomes, although its function is unclear. IMPORTANCE SAR11 clade members are among the most abundant bacteria on Earth. Their study is complicated by their great diversity and difficulties in being grown and manipulated in the laboratory. On the other hand, and due to their extraordinary abundance, metagenomic data sets provide enormous richness of information about these microbes. Given the major role played by phages in the lifestyle and evolution of prokaryotic cells, the contribution of several new bacteriophage genomes preying on this clade opens windows into the infection strategies and life cycle of its viruses. Such strategies could provide models of attack of large-genome phages preying on streamlined aquatic microbes.