Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution

Abstract

The vast majority of cyanophages isolated to date are cyanomyoviruses, a group related to bacteriophage T4. Comparative genome analysis of five cyanomyoviruses, including a newly sequenced cyanophage S-RSM4, revealed a 'core genome' of 64 genes, the majority of which are also found in other T4-like phages. Subsequent comparative genomic hybridization analysis using a pilot microarray showed that a number of 'host' genes are widespread in cyanomyovirus isolates. Furthermore, a hyperplastic region was identified between genes g15-g18, within a highly conserved structural gene module, which contained a variable number of inserted genes that lacked conservation in gene order. Several of these inserted genes were host-like and included ptoX, gnd, zwf and petE encoding plastoquinol terminal oxidase, 6-phosphogluconate dehydrogenase, glucose 6-phosphate dehydrogenase and plastocyanin respectively. Phylogenetic analyses suggest that these genes were acquired independently of each other, even though they have become localized within the same genomic region. This hyperplastic region contains no detectable sequence features that might be mechanistically involved with the acquisition of host-like genes, but does appear to be a site specifically associated with the acquisition process and may represent a novel facet of the evolution of marine cyanomyoviruses.

Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent

“…Phage structural genes can be sequence diverse , and we hypothesize that the dominant sequence type for some structural genes might vary site to site, and this may be the source of our observation of structural genes that are specific to particular sites. Fifteen overrepresented genes have host homologs-that is, are shared phage/host genes with the Genetic diversity in cultured and wild phage L Kelly et al potential to interface with host metabolic pathways and processes (Millard et al, 2009;Sullivan et al, 2010;Sharon et al, 2011;Thompson et al, 2011b;Zeng and Chisholm, 2012). Of particular interest are those related to phosphorous acquisition, because this element can be a defining variable in the structure and function of marine microbial systems and has a key role in shaping the genome content of cyanobacterial hosts (Martiny et al, 2009;Coleman and Chisholm, 2010).…”

“…The gnd/zwf region is variable in cyanophage genomes (Millard et al, 2009), and our previous work indicates that some phage are designed to redirect host metabolism away from carbon fixation and towards nucleotide synthesis via the PPP (Thompson et al, Figure 4 Phylogeny of PhCOG173, a conserved phage gene cluster adjacent to shared phage/host genes. The PhCOG173 cluster, present in both cyanopodovirus and cyanomyovirus genomes (light gray and dark gray bars, respectively) but not host genomes, is found upstream of numerous shared phage/host genes, and phylogenetic groups are associated with different downstream host genes (colored bars).…”

“…Thus it is not surprising that the genomes of all 17 T4-like cyanomyoviruses that infect these cyanobacteria and were available when this study was undertaken (Millard et al, 2009;Sullivan et al, 2010) encode phosphate regulon genes known to be responsive to phosphorus starvation in cyanobacteria (Martiny et al, 2009;Tetu et al, 2009;Sullivan et al, 2010). Some phage genomes encode PstS, a periplasmic high-affinity phosphate-binding protein associated with a phosphate-specific membrane transporter; some encode a homolog of the putative alkaline phosphatase gene phoA.…”

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

“…An emerging paradigm is that viruses also possess auxiliary metabolic genes (AMGs; Breitbart et al, 2007)-'host' genes that may be expressed to augment viral-infected host metabolism and facilitate production of new viruses (reviewed in Breitbart (2012) and Rohwer and Thurber (2009)). Due to the availability of cultures and genomes, AMGs are most extensively explored in marine cyanophages (viruses that infect cyanobacteria) and include genes involved in photosynthesis, carbon metabolism, phosphate metabolism and stress response (Mann et al, 2003;Lindell et al, 2004Lindell et al, , 2005Sullivan et al, 2005;Clokie et al, 2006;Sullivan et al, 2006;Weigele et al, 2007;Dammeyer et al, 2008;Millard et al, 2009;Thompson et al, 2011;Zeng and Chisholm, 2012;Frank et al, 2013). 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).…”

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

“…( Chen and Lu, 2002;Mann et al, 2005;Millard et al, 2009;Sullivan et al, 2010;Huang et al, 2012;Sabehi et al, 2012) and Prochlorococcus spp. (Sullivan et al, 2005(Sullivan et al, , 2009Sullivan et al, 2010;Labrie et al, 2013), as well as one from a myovirus that infects both genera (Weigele et al, 2007).…”