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. 2017 Jun 15:5:e3428.
doi: 10.7717/peerj.3428. eCollection 2017.

Putative archaeal viruses from the mesopelagic ocean

Dean R Vik  1 , Simon Roux  1 , Jennifer R Brum  1 , Ben Bolduc  1 , Joanne B Emerson  1 , Cory C Padilla  2 , Frank J Stewart  2 , Matthew B Sullivan  1   3
Affiliations

Putative archaeal viruses from the mesopelagic ocean

Dean R Vik et al. PeerJ. .

Abstract

Oceanic viruses that infect bacteria, or phages, are known to modulate host diversity, metabolisms, and biogeochemical cycling, while the viruses that infect marine Archaea remain understudied despite the critical ecosystem roles played by their hosts. Here we introduce "MArVD", for Metagenomic Archaeal Virus Detector, an annotation tool designed to identify putative archaeal virus contigs in metagenomic datasets. MArVD is made publicly available through the online iVirus analytical platform. Benchmarking analysis of MArVD showed it to be >99% accurate and 100% sensitive in identifying the 127 known archaeal viruses among the 12,499 viruses in the VirSorter curated dataset. Application of MArVD to 10 viral metagenomes from two depth profiles in the Eastern Tropical North Pacific (ETNP) oxygen minimum zone revealed 43 new putative archaeal virus genomes and large genome fragments ranging in size from 10 to 31 kb. Network-based classifications, which were consistent with marker gene phylogenies where available, suggested that these putative archaeal virus contigs represented six novel candidate genera. Ecological analyses, via fragment recruitment and ordination, revealed that the diversity and relative abundances of these putative archaeal viruses were correlated with oxygen concentration and temperature along two OMZ-spanning depth profiles, presumably due to structuring of the host Archaea community. Peak viral diversity and abundances were found in surface waters, where Thermoplasmata 16S rRNA genes are prevalent, suggesting these archaea as hosts in the surface habitats. Together these findings provide a baseline for identifying archaeal viruses in sequence datasets, and an initial picture of the ecology of such viruses in non-extreme environments.

Keywords: Archaea; Archaeal Virus; Oxygen; Oxygen Minimum Zone; Temperature; Thermoplasmata.

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Conflict of interest statement

The authors declare there are no competing interests.

Figures

Figure 1
Figure 1. Sample locations, environmental features and Archaea 16s rRNA amplicon abundance profiles.
(A) Station 2 and station 6 are located west of Manzanillo Mexico, at the eastern edge of the Eastern Tropical North Pacific. (B) Five samples, denoted by the solid black lines corresponding to various depths, in the surface, upper oxycline, OMZ core, and lower oxycline habitats respectively were selected at each station. Both stations exhibit a sharp reduction in oxygen concentration, reaching a minimum of 1–3 umol kg−1 at roughly 130 m in station 2 and 67 m in station 6. Both stations have a constant reductive thermocline ranging from about 28 °C in the surface to about 6 °C at 1,000 m. Chlorophyll a concentrations are highest in the surface waters and upper oxycline (0.4–0.8 ug/L) and are lowest in the OMZ core and below (∼0.1ug/L). (C) Archaeal 16s rRNA amplicon based relative abundance profiles indicate that Thermoplasmata and Thaumarchaeota, the predominant archaeal phyla present at these sites and have variable distributions on a depth gradient.
Figure 2
Figure 2. vConTact Network analysis of reference of phage and archaeal virus sequences with the ETNP archaeal virus dataset.
(A) The vConTact network developed by using the entire RefSeq archaeal virus (60 sequences) and phage (1,573 sequences) database in conjunction with the ETNP dataset (43 sequences). (B) A focused view of the network comprised of the ETNP archaeal virus populations. The sample habitat at which each VC is found in the highest prevalence is displayed at the top of (B). VCs with red labels are represented in the phylogenetic analysis (Fig. S2).
Figure 3
Figure 3. Synteny maps for each of the putative ETNP archaeal virus cluster (VCs).
(A) VC1. (B) VC2. (C) VC3. (D) VC4. (E) VC5. (F) VC6. Each annotated gene’s taxonomic affiliation is displayed as the colored outline with the bit-score value represented by the weight of the outline. Functional annotations are further depicted as the genes interior color. tBLASTx percent identities among related regions of each population are represented by the gray bar between each population. The portal protein used for verification of the network analysis via phylogenetics is denoted by a star (Fig. S2).
Figure 4
Figure 4. Ecology and relative abundance of putative archaeal viruses.
(A) Evenness (Pielou’s J), alpha diversity (Shannon-Weiner index), and relative abundance, at each sample site and depth. The relative abundance and alpha diversity of putative ETNP archaeal virus populations tracks gradients in oxygen concentration, with the highest abundances found in habitats with high oxygen and vice versa. Viral evenness is high and relatively consistent in each. (B) Relative abundance of archaeal virus populations at each station and sample depth determined by mapping quality trimmed reads to the 43 archaeal virus populations. The units of the abundance measurements are the logarithm (base 10) of the read coverage, normalized by the number of bases in the trimmed read file and contig size. The dendrogram on the x-axis represents the 43 ETNP archaeal virus populations, clustered by relative abundance per sample, and the dendrogram on the y-axis represents the sample locations grouped according to similarities in contig composition. Nodes with approximately unbiased (AU) bootstrapping values greater then 95 (p ≤ 0.05) are displayed with a dot.
Figure 5
Figure 5. Non-metric multidimensional scaling analysis of ETNP putative archaeal virus and Archaea population distribution in relation to environmental variables.
Measurements of temperature, oxygen, salinity, chlorophyll a, and depth were examined to determine which of these features influences the separations among both archaeal virus populations and Archaea in each habitat. Oxygen concentration (A) and Temperature (B) most significantly influenced the ETNP archaeal virus population distribution non-linearly. Oxygen concentration (C) and Temperature (D) also have a linear impact on the distribution of the Archaea. Depth was also found to significantly influence archaeal virus population distributions but this is likely due to a co-variable effect with oxygen and temperature. Salinity and chlorophyll a do not exhibit a significant correlation with the archaeal virus or archaeal population distributions.
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