Genetic diversity and co-occurrence patterns of marine cyanopodoviruses and picocyanobacteria.

Picocyanobacteria Prochlorococcus and Synechococcus are abundant in the global oceans and subject to active viral infection. In this study, the genetic diversity of picocyanobacteria and the genetic diversity of cyanopodoviruses were synchronously investigated along water columns in the equatorial Indian Ocean and over a seasonal time course in the coastal Sanya Bay, South China Sea. Using the 16S-23S rRNA internal transcribed spacer (ITS)-based clone library and quantitative PCR (qPCR) analyses, the picocyanobacterial community composition and abundance were determined. Sanya Bay was dominated by Glade II Synechococcus during all the seasons, and a typical population shift from high-light-adapted Prochlorococcus to low-light-adapted Prochlorococcus was found along the vertical profiles. Strikingly, the DNA polymerase gene sequences of cyanopodoviruses revealed a much greater genetic diversity than we expected. Nearly one-third of the phylogenetic groups were newly described here. No apparent seasonal pattern was observed for the Sanya Bay picocyanobacterial or cyanopodoviral communities. Different dominant cyanopodovirus lineages were identified for the coastal area, upper euphotic zone, and middle-to-lower euphotic zone of the open ocean. Diversity indices of both picocyanobacteria and cyanopodoviruses were highest in the middle euphotic zone and both were lower in the upper euphotic zone, reflecting a host-virus interaction. Cyanopodoviral communities differed significantly between the upper euphotic zone and the middle-to-lower euphotic zone, showing a vertical pattern similar to that of picocyanobacteria. However, in the surface waters of the open ocean, cyanopodoviruses exhibited no apparent biogeographic pattern, differing from picocyanobacteria. This study demonstrates correlated distribution patterns of picocyanobacteria and cyanopodoviruses, as well as the complex biogeography of cyanopodoviruses. IMPORTANCE Picocyanobacteria are highly diverse and abundant in the ocean and display remarkable global biogeography and a vertical distribution pattern. However, how the diversity and distribution of picocyanobacteria affect those of the viruses that infect them remains largely unknown. Here we synchronously analyzed the community structures of cyanopodoviruses and picocyanobacteria at spatial and temporal scales. Both spatial and temporal variations of cyanopodoviral communities can be linked to those of picocyanobacteria. The coastal area, upper euphotic zone, and middle-to-lower euphotic zone of the open ocean have distinct cyanopodoviral communities, showing horizontal and vertical variation patterns closely related to those of picocyanobacteria. These findings emphasize the driving force of host community in shaping the biogeographic structure of viruses. Our work provides important information for future assessments of the ecological roles of viruses and hosts for each other.