Twelve previously unknown phage genera are ubiquitous in global oceans

Abstract

Viruses are fundamental to ecosystems ranging from oceans to humans, yet our ability to study them is bottlenecked by the lack of ecologically relevant isolates, resulting in "unknowns" dominating culture-independent surveys. Here we present genomes from 31 phages infecting multiple strains of the aquatic bacterium Cellulophaga baltica (Bacteroidetes) to provide data for an underrepresented and environmentally abundant bacterial lineage. Comparative genomics delineated 12 phage groups that (i) each represent a new genus, and (ii) represent one novel and four wellknown viral families. This diversity contrasts the few well-studied marine phage systems, but parallels the diversity of phages infecting human-associated bacteria. Although all 12 Cellulophaga phages represent new genera, the podoviruses and icosahedral, nontailed ssDNA phages were exceptional, with genomes up to twice as large as those previously observed for each phage type. Structural novelty was also substantial, requiring experimental phage proteomics to identify 83% of the structural proteins. The presence of uncommon nucleotide metabolism genes in four genera likely underscores the importance of scavenging nutrient-rich molecules as previously seen for phages in marine environments. Metagenomic recruitment analyses suggest that these particular Cellulophaga phages are rare and may represent a first glimpse into the phage side of the rare biosphere. However, these analyses also revealed that these phage genera are widespread, occurring in 94% of 137 investigated metagenomes. Together, this diverse and novel collection of phages identifies a small but ubiquitous fraction of unknown marine viral diversity and provides numerous environmentally relevant phage-host systems for experimental hypothesis testing. model systems | phage genomics | phage taxonomy | queuosine biosynthesis | prophage

Polar freshwater cyanophage S-EIV1 represents a new widespread evolutionary lineage of phages

“…This has been shown recently with previously unknown groups of viruses isolated on Pelagibacter ubique (Zhao et al, 2013), a bacterium of SAR116 clade (Kang et al, 2013) and Cellulophaga baltica (Holmfeldt et al, 2013). Similarly, most cyanophages have been isolated using a few strains of Synechococcus spp.…”

“…Similarly, S-EIV1 shares negligible genetic similarity with the large podoviruses that infect Cellulophaga baltica (Holmfeldt et al, 2013), including genes encoding the structural proteins. In fact, sequences encoding known phage structural proteins (that is, capsid, tail tube, portal or tail fiber) were not found within the S-EIV1 genome, with the exception of the terminase large subunit and a viral morphogenesis protein classified with HHpred, providing further evidence that S-EIV1 is distinct from podoviruses and represents a previously unknown phage lineage.…”

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

“…First, glutaredoxin, the most abundant Fe-S cluster protein in the POV data set, reduces ribonucleotide reductase and may augment the conversion of RNA to DNA to produce genomes of viral progeny (Dwivedi et al, 2013;Holmfeldt et al, 2013). Second, additional POV-encoded genes suggest that viruses mediate host stress response through (i) producing Fe-S cluster containing polyamines including adenosylmethionine decarboxylase (speD) or methionine adenosyltransferase (metK) (Imai et al, 2004;Igarashi and Kashiwagi, 2010), or (ii) degrading sigma factors via Fe-S protein degradation genes clpX and clpP (Hengge, 2008;Calhoun and Kwon, 2011).…”

Illuminating structural proteins in viral “dark matter” with metaproteomics

“…Computationally, artificial neural networks have been used to predict viral capsid and tail proteins from metagenomic data, which has been validated through in vivo expression and visualization of four putative viral structural genes (17). Experimentally, divergent structural proteins from cultivated viral isolates have been annotated using mass spectrometry (MS)-based proteomics (13,(18)(19)(20). Metaproteomics has now emerged as a powerful tool to investigate microbial communities (21,22), and here we apply this approach to marine viral communities to identify virionassociated proteins and facilitate annotation of the structural components of viral dark matter, generating new insights regarding the structural proteins in natural viral communities.…”