Marine Cyanophages Demonstrate Biogeographic Patterns throughout the Global Ocean

Myoviruses and podoviruses that infect cyanobacteria are the two major groups of marine cyanophages, but little is known of how their phylogenetic lineages are distributed in different habitats. In this study, we analyzed the phylogenetic relationships of cyanopodoviruses and cyanomyoviruses based on the existing genomes. The 28 cyanomyoviruses were classified into four clusters (I to IV), and 19 of the 20 cyanopodoviruses were classified into two clusters, MPP-A and MPP-B, with four subclusters within cluster MPP-B. These genomes were used to recruit cyanophage-like fragments from microbial and viral metagenomes to estimate the relative abundances of these cyanophage lineages. Our results showed that cyanopodoviruses and cyanomyoviruses are both abundant in various marine environments and that clusters MPP-B, II and III appear to be the most dominant lineages. Cyanopodoviruses and cluster I and IV cyanomyoviruses exhibited habitat-related variability in their relative levels of abundance, while cluster II and III cyanomyoviruses appeared to be consistently dominant in various habitats. Multivariate analyses showed that reads that mapped to Synechococcus phages and Prochlorococcus phages had distinct distribution patterns that were significantly correlated to those of Synechococcus and Prochlorococcus, respectively. The Mantel test also revealed a strong correlation between the community compositions of cyanophages and picocyanobacteria. Given that cyanomyoviruses tend to have a broad host range and some can cross-infect Synechococcus and Prochlorococcus, while cyanopodoviruses are commonly host specific, the observation that their community compositions both correlated significantly with that of picocyanobacteria was unexpected. Although cyanomyoviruses and cyanopodoviruses differ in host specificity, their biogeographic distributions are likely both constrained by the picocyanobacterial community.