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. 2006 Nov;4(11):e368.
doi: 10.1371/journal.pbio.0040368.

The marine viromes of four oceanic regions

Florent E Angly  1 , Ben Felts, Mya Breitbart, Peter Salamon, Robert A Edwards, Craig Carlson, Amy M Chan, Matthew Haynes, Scott Kelley, Hong Liu, Joseph M Mahaffy, Jennifer E Mueller, Jim Nulton, Robert Olson, Rachel Parsons, Steve Rayhawk, Curtis A Suttle, Forest Rohwer
Affiliations

The marine viromes of four oceanic regions

Florent E Angly et al. PLoS Biol. 2006 Nov.

Abstract

Viruses are the most common biological entities in the marine environment. There has not been a global survey of these viruses, and consequently, it is not known what types of viruses are in Earth's oceans or how they are distributed. Metagenomic analyses of 184 viral assemblages collected over a decade and representing 68 sites in four major oceanic regions showed that most of the viral sequences were not similar to those in the current databases. There was a distinct "marine-ness" quality to the viral assemblages. Global diversity was very high, presumably several hundred thousand of species, and regional richness varied on a North-South latitudinal gradient. The marine regions had different assemblages of viruses. Cyanophages and a newly discovered clade of single-stranded DNA phages dominated the Sargasso Sea sample, whereas prophage-like sequences were most common in the Arctic. However most viral species were found to be widespread. With a majority of shared species between oceanic regions, most of the differences between viral assemblages seemed to be explained by variation in the occurrence of the most common viral species and not by exclusion of different viral genomes. These results support the idea that viruses are widely dispersed and that local environmental conditions enrich for certain viral types through selective pressure.

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Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Sampling Sites
The circles represent the sampling locations in the Sargasso Sea (SAR), Gulf of Mexico (GOM), British Columbia (BBC), and the Arctic Ocean. The number of samples taken at each location and combined for sequencing, as well as the date and depth range, are shown in the boxes.
Figure 2
Figure 2. Composition of the Assemblage Genome Sequences as Determined by Similarity to Known DNA and Protein Sequences
(A) The percent of “known” sequences compared to the SEED and environmental databases. A sequence was considered “known” if it had a significant similarity (E < 10−5) to the SEED, else “environmental” if it had a similarity to any environmental database, and else “unknown”. (B) Breakdown of the “known” sequences into viral (both eukaryotic and bacteriophages), prophage, Bacteria, Archaea, or Eukarya.
Figure 3
Figure 3. Distribution of Similarities and Assembly Controls
(A) Distribution of similarities between the four metagenome samples to the P. marinus φ P-SSP7 and Roseobacteria SIO67 φ SIO1 genomes (as determined by BLASTN analysis). The green bars represent the average number of sequences averaged over 100 bp windows. (B) Comparison of fragments from the Sargasso Sea metagenome against the consensus ssDNA chp1-like microphage genome. The consensus from this assembly is in the Protocol S1. (C) PCR verification of chp1-like microphages in original SAR sample. PCR primers were designed based on a consensus sequence from the assembly shown in (B). SAR1 is a ~900-bp fragment and SAR2 is a ~1,500-bp fragment.
Figure 4
Figure 4. Types of Phages in the Four Metagenomes
A new version of the Phage Proteomic Tree (left panel) was constructed from 510 complete phage and prophage genomes using the previously described method [23]. The metagenomic sequences were compared to the phage on the Phage Proteomic Tree using TBLASTX, and the colored bars on the right represent significant similarities (E-value < 0.0001). Names of prophages are in red and the Prochlorococcus phage genomes are in green. An electronic version of the tree and a FASTA list of phage and prophage genomes used to make the tree are available at the SDSU Center for Universal Microbe Sequencing website (http://scums.sdsu.edu/phage/Oceans).
Figure 5
Figure 5. Relationship between Geographic and Genetic Distances of Marine Viral Assemblages
In addition to the four metagenomes sequenced for this study, the previous viral metagenomes from the San Diego area (California coast) were also included in this analysis [10]. There was a significant correlation of 3.28 × 10−5 ΦST / km (Mantel test, Z = −78.9, p < 0.017, r = 0.585).
Figure 6
Figure 6. Monte Carlo Simulation of Cross-Contigs between Metagenomic Samples
(A) For the intersample analysis, the maximum likelihood occurred at 35% fraction permuted and 100% fraction shared. (B) The maximum likelihood was between 0% and 0.5% fraction permuted and 85% and 95 % fraction shared for the intrasample controls.
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