Associations between picocyanobacterial ecotypes and cyanophage host genes across ocean basins and depth.

Background: Cyanophages, viruses that infect cyanobacteria, are globally abundant in the ocean's euphotic zone and are a potentially important cause of mortality for marine picocyanobacteria. Viral host genes are thought to increase viral fitness by either increasing numbers of genes for synthesizing nucleotides for virus replication, or by mitigating direct stresses imposed by the environment. The encoding of host genes in viral genomes through horizontal gene transfer is a form of evolution that links viruses, hosts, and the environment. We previously examined depth profiles of the proportion of cyanophage containing various host genes in the Eastern Tropical North Pacific Oxygen Deficient Zone (ODZ) and at the subtropical North Atlantic (BATS). However, cyanophage host genes have not been previously examined in environmental depth profiles across the oceans. Methodology: We examined geographical and depth distributions of picocyanobacterial ecotypes, cyanophage, and their viral-host genes across ocean basins including the North Atlantic, Mediterranean Sea, North Pacific, South Pacific, and Eastern Tropical North and South Pacific ODZs using phylogenetic metagenomic read placement. We determined the proportion of myo and podo-cyanophage containing a range of host genes by comparing to cyanophage single copy core gene terminase (terL). With this large dataset (22 stations), network analysis identified statistical links between 12 of the 14 cyanophage host genes examined here with their picocyanobacteria host ecotypes. Results: Picyanobacterial ecotypes, and the composition and proportion of cyanophage host genes, shifted dramatically and predictably with depth. For most of the cyanophage host genes examined here, we found that the composition of host ecotypes predicted the proportion of viral host genes harbored by the cyanophage community. Terminase is too conserved to illuminate the myo-cyanophage community structure. Cyanophage cobS was present in almost all myo-cyanophage and did not vary in proportion with depth. We used the composition of cobS phylotypes to track changes in myo-cyanophage composition. Conclusions: Picocyanobacteria ecotypes shift with changes in light, temperature, and oxygen and many common cyanophage host genes shift concomitantly. However, cyanophage phosphate transporter gene pstS appeared to instead vary with ocean basin and was most abundant in low phosphate regions. Abundances of cyanophage host genes related to nutrient acquisition may diverge from host ecotype constraints as the same host can live in varying nutrient concentrations. Myo-cyanophage community in the anoxic ODZ had reduced diversity. By comparison to the oxic ocean, we can see which cyanophage host genes are especially abundant (nirA, nirC, and purS) or not abundant (myo psbA) in ODZs, highlighting both the stability of conditions in the ODZ and the importance of nitrite as an N source to ODZ endemic LLV Prochlorococcus.

Cyanophage host-derived genes reflect contrasting selective pressures with depth in the oxic and anoxic water column of the Eastern Tropical North Pacific.

Cyanophages encode host-derived genes that may increase their fitness. We examined the relative abundance of 18 host-derived cyanophages genes in metagenomes and viromes along depth profiles from the Eastern Tropical North Pacific Oxygen Deficient Zone (ETNP ODZ) where Prochlorococcus dominates a secondary chlorophyll maximum within the ODZ. Cyanophages at the oxic primary chlorophyll maximum encoded genes related to light and phosphate stress (psbA, psbD and pstS in T4-like and psbA in T7-like), but the proportion of cyanophage with these genes decreased with depth. The proportion of cyanophage with purine biosynthesis genes increased with depth in T4-like, but not T7-like cyanophages. No additional host-derived genes were found in deep T7-like cyanophages, suggesting that T4-like and T7-like cyanophages have different host-derived gene acquisition strategies, possibly linked to their different genome packaging mechanisms. In contrast to the ETNP, in the oxic North Atlantic T4-like cyanophages encoded psbA and pstS throughout the euphotic zone. Differences in pstS between the ETNP and the North Atlantic stations were consistent with differences in phosphate concentrations in those regimes. We suggest that the low proportion of cyanophage with psbA within the ODZ reflects the stably stratified low-light conditions occupied by their hosts, a Prochlorococcus ecotype endemic to ODZs.