Two new clades of T7-like cyanophages: diversity, distribution and infection patterns based on omics data

Cyanobacteria play a significant role in global biogeochemical cycles, including carbon fixation and oxygen production. Among them, marine picocyanobacteria Prochlorococcus and Synechococcus constitute the most numerically abundant group of photosynthetic organisms on Earth. They are dominant in oligotrophic regions and contribute a quarter of primary production in the ocean. Picocyanobacterial distribution depends on abiotic factors, e.g. light, temperature, and nutrients, as well as biotic mortality factors, such as grazers and viral infection. Viruses also impact the diversity of picocyanobacteria during their coevolution. Infection of cyanobacteria by phages ends in lysis and release of organic matter from cells to the water column. The T7-like cyanophage family is one of two main virus families infecting marine picocyanobacteria. Two groups of T7-like cyanophages were known until recently: clades A and B. They have various distribution, infection properties and patterns, resulting in differential impacts on picocyanobacterial populations. In 2023 a new group of T7-like cyanophages was discovered, and was named clade C. However, only two genotypes of the novel group were known, both isolated on Prochlorococcus. In this study we investigated the diversity within the new group using assembled environmental sequences. We also estimated the relative abundance and infection of this group and compared them with other T7-like cyanophages clades along a transect in the North Pacific Ocean and over the spring period or from winter mixing to summer stratification in the Red Sea. For this we used viromic and cellular metagenomic data to determine relative abundance of free-living viruses and gain an indication of infection, respectively. We found that the new group actually consists of two distinct clades, which we renamed as clades C and D. Clade D is more diverse than clade C. In the North Pacific Ocean both clades were relatively more abundant in the North Pacific Subtropical Gyre and decreased towards the north. In some samples clade D recruited more than 40% of T7-like cyanophage viromic reads. In the Red Sea the relative abundance of both clades increased towards the summer. In both regions clade D was generally more abundant that clade C, and the abundances of clades C and D followed the abundances of Prochlorococcus. This study provides new insights into the diversity, spatial distribution and seasonal dynamics of two new clades of T7-like cyanophages. It demonstrates that clade D could be an important viral group impacting primary production and biogeochemical cycles in the oligotrophic oceans.