Bacteriophage Distributions and Temporal Variability in the Ocean’s Interior

Abstract

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.

Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

“…4). The depthstratified viral community is analogous to that reported from ocean (Hurwitz et al, 2015;Mizuno et al, 2016;Paez-Espino et al, 2016;López-Pérez et al, 2017;Luo et al, 2017) and likely reflects the depth-stratified community of bacterioplankton (Okazaki and Nakano, 2016) (Table S4). The viral community was generally stable in the hypolimnion (the Bray-Curtis dissimilarity of the communities between consecutive months = 0.21-0.34; except for September to October and December to January as discussed later) compared to the epilimnetic community (0.54-0.68) (Figs.…”

“…Since no integrase gene was found in their genomes, they may have existed in a host's cell in an extrachromosomal or pseudolysogenic manner. As proposed for the deep ocean (Weinbauer et al, 2003;Paul, 2008;Mizuno et al, 2016;Luo et al, 2017), the lysogenic strategy in deeper water likely results from low bacterioplankton productivity, which is insufficient to support lytic viral propagation. Lytic induction can be triggered by environmental stressors such as pH, temperature, nutrients, oxidative stress, and solar radiation (Weinbauer, 2004;Howard-Varona et al, 2017).…”

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

“…). The depth‐stratified viral community is analogous to that reported from ocean (Hurwitz et al ., ; Mizuno et al ., ; Paez‐Espino et al ., ; López‐Pérez et al ., ; Luo et al ., ) and likely reflects the depth‐stratified community of bacterioplankton (Okazaki and Nakano, ) (Supporting Information Table S4).…”

“…As no integrase gene was found in their genomes, they may have existed in a host's cell in an extrachromosomal or pseudolysogenic manner. As proposed for the deep ocean (Weinbauer et al ., ; Paul, ; Mizuno et al ., ; Luo et al ., ), the lysogenic strategy in deeper water likely results from low bacterioplankton productivity, which is insufficient to support lytic viral propagation. Lytic induction can be triggered by environmental stressors such as pH, temperature, nutrients, oxidative stress and solar radiation (Weinbauer, ; Howard‐Varona et al ., ).…”

Viral Invasion Fitness Across a Continuum from Lysis to Latency

“…More than a decade ago, studies of marine, hydrothermal, and soil environments suggested that lysogeny could be more prevalent than assumed based on culture-based analysis of virus-microbe interactions [15][16][17][18]. This evidence has been augmented by recent studies identifying viral dark matter -including integrated and extrachromosomal viral sequences -in microbial genomes [19][20][21]. Yet, despite increasing evidence of the relevance of persistent infections in situ the ecological study of phage has not integrated a common metric to compare the contextdependent fitness of lytic, temperate, and other chronic viral strategies.…”