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. 2017 Nov 28;8(6):e01903-17.
doi: 10.1128/mBio.01903-17.

Bacteriophage Distributions and Temporal Variability in the Ocean's Interior

Affiliations

Bacteriophage Distributions and Temporal Variability in the Ocean's Interior

Elaine Luo et al. mBio. .

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.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.

Keywords: bacteriophages; bacterioplankton; marine microbiology; microbial ecology; microbial oceanography.

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Figures

FIG 1
FIG 1
Depth profiles of known and novel phage ALOHA viral contigs assigned using four reference databases: known phages in RefSeq75 protein database and three previously sequenced viral metagenomes. Phages are identified with a cutoff of >50% genes with >60% average amino acid identity to a reference database genome. (a) Proportion of contigs with hits to known phages in RefSeq75, other viromes, and novel phages. (b) Subset of hits to RefSeq75. (c) Subset of hits to other viromes: uvMED from the Mediterranean (15), Global Ocean Viromes (GOV) from Tara Oceans (14), and Earth viromes (EV) from human, terrestrial, and marine environments (27). The number of contigs in each category is shown in the legend. Proportion is normalized by total nucleotides mapped to each contig. Error bars show standard errors, which are summed among groups in stacked bars.
FIG 2
FIG 2
Coverage profiles of 129 ALOHA viral contigs through depth and time. Each node on the top dendrogram and its associated column represent one contig, while each row represents one of 83 total samples. The height of the black column within a cell represents the mean coverage (second and third quartiles) of a contig in a given sample. The full bar height of each sample layer is log scaled to the maximum coverage in a given sample. Sample layers are ordered by depth from 25 to 1,000 m, shown on the right. Within each depth bin, samples are ordered by time from August 2010 to December 2011, shown on the left. Contigs are clustered by differential coverage, with manual binning into five groups on the bottom. Across the top, homology to known phages in the RefSeq75 protein database and other viral metagenomes was assigned based on >50% genes hitting at >60% average amino acid identity.
FIG 3
FIG 3
Cluster analysis of phage-specific versus cellular genes identified in the Station ALOHA time-series nonredundant gene catalog. Each edge on the trees represents one sample, and corresponding samples are shown with connecting lines between the two dendrograms.
FIG 4
FIG 4
Temporal variability of assembled viral contigs increased with depth. (a) Relative abundance of the most abundant ALOHA viral contigs at 25 and 1,000 m. Each row represents one of the 13 most abundant ALOHA viral contigs for each depth bin, with size indicated in kilobase pairs (kbp). Asterisks represent contigs containing one or more prophage markers (PFAM bit score of >30 to integrase, CI repressor, Cro, or excisionase). Relative abundance is scaled by area. (b) Mean-normalized variance of relative abundance through time calculated for each contig.
FIG 5
FIG 5
Depth profile of prophage marker proteins identified in the Station ALOHA time-series nonredundant gene catalog (domain bit score of >50) using hidden Markov models generated with manually curated sets of viral marker proteins from NCBI. Each circle represents a sample mean, and each vertical bar represents a depth mean. Depth profile of prophage markers integrase (a), CI repressor (b), and excisionase (c). The fold increase of prophage markers with respect to surface mean is calculated using coverage of marker proteins normalized to coverage of capsid proteins.

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