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. 2017 May 8;27(9):1362-1368.
doi: 10.1016/j.cub.2017.03.052. Epub 2017 Apr 27.

Novel Abundant Oceanic Viruses of Uncultured Marine Group II Euryarchaeota

Alon Philosof  1 , Natalya Yutin  2 , José Flores-Uribe  3 , Itai Sharon  4 , Eugene V Koonin  2 , Oded Béjà  5
Affiliations

Novel Abundant Oceanic Viruses of Uncultured Marine Group II Euryarchaeota

Alon Philosof et al. Curr Biol. .

Abstract

Marine group II Euryarchaeota (MG-II) are among the most abundant microbes in oceanic surface waters [1-4]. So far, however, representatives of MG-II have not been cultivated, and no viruses infecting these organisms have been described. Here, we present complete genomes for three distinct groups of viruses assembled from metagenomic sequence datasets highly enriched for MG-II. These novel viruses, which we denote magroviruses, possess double-stranded DNA genomes of 65 to 100 kilobases in size that encode a structural module characteristic of head-tailed viruses and, unusually for archaeal and bacterial viruses, a nearly complete replication apparatus of apparent archaeal origin. The newly identified magroviruses are widespread and abundant and therefore are likely to be major ecological agents.

Keywords: DNA polymerase; archaea; marine; phage; replication; virus.

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Figures

Figure 1
Figure 1
Unrooted Maximum Likelihood Phylogenetic Trees of Conserved Magrovirus Genes (A) Major capsid protein (MCP). (B) DNA polymerase B (DNAP). (C) Archaeo-eukaryotic primase (AEP). (D) Chaperonins (thermosome subunit and GroEL). Metagenome-assembled complete or nearly complete genomes (MAGs) of magrovirus from the Red Sea and Tara Oceans metagenomes are marked with red and light red circles, respectively. Bootstrap support values greater than 90 are marked with gray circles. See also Figures S2 and S3.
Figure 2
Figure 2
Genome Organization in Different Groups of Magroviruses and Haloviruses For each group, detailed genome schemes of the replicative gene block (left, yellow to red) and the structural gene block (right, different shades of blue) are shown. Homologous genes with predicted functions are shown using color code (see key at the bottom). Green arrows indicate thermosome genes, and gray arrows indicate hypothetical proteins. Split DNAP genes from group B1 are marked with a narrow black arrow pointing to the regions between the split genes. See also Figure S1 and Table S1.
Figure 3
Figure 3
Global Abundance of Magroviruses and MG-II and/or MG-III (A) Recruitment plots of representatives from different magrovirus groups (A: MAG 154566, B1: MAG 154680, B2: MAG SAMEA2620879_23, C: MAG 155057), using reads (viral fraction) from surface waters (top 5 m) from the Red Sea and different Tara Oceans stations. (B) Non-metric multidimensional scaling (NMDS) plot of sampling sites magrovirus abundance. Circle diameter indicates magrovirus abundance at a specific site. MG-II abundance is represented by a gradient of white to red contour lines. A linear response between the magrovirus abundance ordination and the MG-II abundance variable is represented by fitted contours that are equally spaced parallel lines perpendicular to the MG-II abundance vector (R-sq.[adj] = 0.432; deviance explained = 48%; p value = 4.82e−10). Region abbreviations are as follows: IO, Indian Ocean; RS, Red Sea; SO, Southern Ocean; MS, Mediterranean Sea; NPO, North Pacific Ocean; SAO, South Atlantic Ocean; SPO, South Pacific Ocean.
Figure 4
Figure 4
Total Abundance of Magroviruses The abundance of the Magrovirus reads in Red Sea samples and all Tara Oceans microbiomes [21] and viromes [18] is shown along with the abundances of the putative host MG-II, marine group I Crenarchaeota, marine Cyanobacteria (Synechococcus and Prochlorococcus) and their phages, SAR11 bacteria and their phages, and SAR116 and their phages. Plots for halovirus and representatives from cultured Euryarchaeota are not shown as the signals were close to zero. Horizontal axis: the normalized count (genome fragments per kilobase reference sequence per million library reads [GFPM]; see Supplemental Experimental Procedures). Vertical axis: the sampling stations.
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