Bacteriophage Distributions and Temporal Variability in the Ocean's Interior

Bacteriophages are numerically the most abundant DNA-containing entities in the oligotrophic ocean, yet how specific phage populations vary over time and space remains to be fully explored. Here, we conducted a metagenomic time-series survey of double-stranded DNA phages throughout the water column in the North Pacific Subtropical Gyre, encompassing 1.5 years from depths of 25 to 1,000 m. Viral gene sequences were identified in assembled metagenomic samples, yielding an estimated 172,385 different viral gene families. Viral marker gene distributions suggested that lysogeny was more prevalent at mesopelagic depths than in surface waters, consistent with prior prophage induction studies using mitomycin C. A total of 129 ALOHA viral genomes and genome fragments from 20 to 108 kbp were selected for further study, which represented the most abundant phages in the water column. Phage genotypes displayed discrete population structures. Most phages persisted throughout the time-series and displayed a strong depth structure that mirrored the stratified depth distributions of co-occurring bacterial taxa in the water column. Mesopelagic phages were distinct from surface water phages with respect to diversity, gene content, putative life histories, and temporal persistence, reflecting depth-dependent differences in host genomic architectures and phage reproductive strategies. The spatiotemporal distributions of the most abundant open-ocean bacteriophages that we report here provide new insight into viral temporal persistence, life history, and virus-host-environment interactions throughout the open-ocean water column. IMPORTANCE The North Pacific Subtropical Gyre represents one of the largest biomes on the planet, where microbial communities are central mediators of ecosystem dynamics and global biogeochemical cycles. Critical members of these communities are the viruses of marine bacteria, which can alter microbial metabolism and significantly influence their survival and productivity. To better understand these viral assemblages, we conducted genomic analyses of planktonic viruses over a seasonal cycle to ocean depths of 1,000 m. We identified 172,385 different viral gene families and 129 unique virus genotypes in this open-ocean setting. The spatiotemporal distributions of the most abundant open-ocean viruses that we report here provide new insights into viral temporal variability, life history, and virus-host-environment interactions throughout the water column.