Comparative metagenomics of microbial traits within oceanic viral communities

Abstract

Viral genomes often contain genes recently acquired from microbes. In some cases (for example, psbA) the proteins encoded by these genes have been shown to be important for viral replication. In this study, using a unique search strategy on the Global Ocean Survey (GOS) metagenomes in combination with marine virome and microbiome pyrosequencing-based datasets, we characterize previously undetected microbial metabolic capabilities concealed within the genomes of uncultured marine viral communities. A total of 34 microbial gene families were detected on 452 viral GOS scaffolds. The majority of auxiliary metabolic genes found on these scaffolds have never been reported in phages. Host genes detected in viruses were mainly divided between genes encoding for different energy metabolism pathways, such as electron transport and newly identified photosystem genes, or translation and post-translation mechanism related. Our findings suggest previously undetected ways, in which marine phages adapt to their hosts and improve their fitness, including translation and post-translation level control over the host rather than the already known transcription level control.

Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome

“…Given that sufA is homologous to iscA (Ollagnier-de-Choudens et al, 2004), it cannot be confirmed whether one or both genes are present; however, both function as scaffold proteins in Fe-S cluster assembly indicating that this is likely important in viruses. Another such biogenesis gene (sufE) was also detected and has been previously documented in viromes (Sharon et al, 2011), but occurred in only 12 of the 16 POV photic zone viromes. In addition, three PCE genes suggest that Pacific Ocean viruses also augment Fe-S protein folding (ATP-dependent molecular chaperone, (clpX)) and degradation of Fe-S cluster proteins (serine protease (clpP) and DNA-binding ATPdependent protease La (lon) (Rouault and Tong, 2005)), although their functions may be generalizable to other proteins.…”

“…Seven of these were observed previously in viral genomes and metagenomes including thyA, def (PDF), dnaB, dnaG, xerC, ligD and dam (Scherzinger et al, 1977;Yonesaki, 1994;Subramanya et al, 1996;Huber and Waldor, 2002;Pitcher et al, 2006;Sullivan et al, 2010;Sharon et al, 2011). The two that are newly described for viruses include genes encoding an endonuclease (uvdE) and a phosphate transport protein (phoU).…”

“…Although viruses obtain and maintain such AMGs for their own fitness advantage, it is probable-as in the psbA and psbD cases (Sullivan et al, 2006)-that independently evolving viralencoded AMGs also serve as a source of genetic novelty that periodically alters host metabolic function and evolution. Given so many newly discovered AMGs (this study and ; Sharon et al (2011)) and the fact that a large fraction of microbes are infected by viruses at any given time (Wommack and Colwell, 2000), suggests that cells should be modeled separately as 'infected' and 'uninfected' as their metabolic output undoubtedly sharply differs.…”

“…AMGs have also been observed in other cultivated viral isolates including genes for sugar metabolism, lipid-fatty acid metabolism and signalling (Derelle et al, 2008). Further, culture-independent metagenomic surveys have identified additional AMGs involved in motility, anti-oxidation, photosystem I, energy metabolism and iron-sulphur clusters (Yooseph et al, 2007;Dinsdale et al, 2008;Sharon et al, 2009Sharon et al, , 2011, with recent, focused pathway analysis expanding these ocean virus-encoded AMG lists to include nearly all of central carbon metabolism .…”

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

“…similar to a domain from the "metabolism" category) were then selected for further study because of their central role in sulfur (dsrC and soxYZ) or nitrogen (P-II, amoC) cycle, and the fact that these had never been detected in a surface ocean viral genome so far (dsrC/tusE-like genes have been detected in deep water viruses 14,29 ). To evaluate if an AMG was "known", a list of PFAM domain detected in NCBI RefSeqVirus and Environmental Phages was computed based on a similar hmmsearch comparison (threshold of 40 on bit score and 0.001 on e-value), and augmented by manual annotation of AMGs from 24,82 . The complete list of PFAM domains detected in GOV viral contigs is available as Supplementary Table 5.…”