Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage–host genetic exchanges

Abstract

Investigating the interactions between marine cyanobacteria and their viruses (phages) is important towards understanding the dynamic of ocean's primary productivity. Genome sequencing of marine cyanophages has greatly advanced our understanding about their ecology and evolution. Among 24 reported genomes of cyanophages that infect marine picocyanobacteria, 17 are from cyanomyoviruses and six from cyanopodoviruses, and only one from cyanosiphovirus (Prochlorococcus phage P-SS2). Here we present four complete genome sequences of siphoviruses (S-CBS1, S-CBS2, S-CBS3 and S-CBS4) that infect four different marine Synechococcus strains. Three distinct subtypes were recognized among the five known marine siphoviruses (including P-SS2) in terms of morphology, genome architecture, gene content and sequence similarity. Our study revealed that cyanosiphoviruses are genetically diverse with polyphyletic origin. No core genes were found across these five cyanosiphovirus genomes, and this is in contrast to the fact that many core genes have been found in cyanomyovirus or cyanopodovirus genomes. Interestingly, genes encoding three structural proteins and a lysozyme of S-CBS1 and S-CBS3 showed homology to a prophage-like genetic element in two freshwater Synechococcus elongatus genomes. Re-annotation of the prophage-like genomic region suggests that S. elongatus may contain an intact prophage. Cyanosiphovirus genes involved in DNA metabolism and replication share high sequence homology with those in cyanobacteria, and further phylogenetic analysis based on these genes suggests that ancient and selective genetic exchanges occurred, possibly due to past prophage integration. Metagenomic analysis based on the Global Ocean Sampling database showed that cyanosiphoviruses are present in relatively low abundance in the ocean surface water compared to cyanomyoviruses and cyanopodoviruses.

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).…”

“…Most cyanophage isolates are myoviruses with genome size ranges from 161 to 252 kb, and share core genes involved in virion structure, DNA replication and host-derived genes with T4-like phage (Mann et al, 2005;Millard et al, 2009;Sullivan et al, 2010) A number of sequenced marine cyanophages are also podoviruses, having genomes between 42 kb and 47 kb, and sharing similar genome architecture, as well as core genes with T7-like phages, including genes involved in virion structure, DNA replication and that are host-derived (Chen and Lu, 2002;Sullivan et al, 2005;Labrie et al, 2013). The few sequenced marine cyanophages that are siphoviruses have genome sizes between 30 and 108 kb (Sullivan et al, 2005;Huang et al, 2012;Ponsero et al, 2013), and, although divergent from other siphoviruses, they share several functional genes with lambda-like phages.…”

Unraveling the genome structure of cyanobacterial podovirus A-4L with long direct terminal repeats

“…As a preface to gain insight into the biological properties of cyanophages and their interactions with cyanobacterial hosts at the molecular level, it is necessary to obtain their complete genome sequences. Since the first total genome sequence of a Synechococcus cyanophage P60 was reported in 2002, more than 40 cyanophages from different species of cyanobacteria have been characterized at the genome level (Chen and Lu, 2002;Liu et al, 2008;Huang et al, 2012;Dreher et al, 2011;Gao et al, 2012;Labrie et al, 2013). Furthermore, some cyanophages have been reported to contain special genes, such as photosynthesis-related genes, carbon metabolism genes and phosphate stress genes, and these genes are speculated to play defining functional roles in cyanobacterial virus-host interactions (Lindell et al, 2004(Lindell et al, , 2005Sullivan et al, 2005;Gao et al, 2012).…”

Reconstruction of Novel Cyanobacterial Siphovirus Genomes from Mediterranean Metagenomic Fosmids

“…Additionally, four more new cyanosiphoviruses (S-CBS1, S-CBS2, S-CBS3, and S-CBS-4), infecting Synechococcus, are now available (24). Analysis of these phages revealed genetically diverse and polyphyletic genomes, and apart from some typical structural phage genes (e.g., terminase), no host photosystemrelated genes that are frequently found in podoviruses and myoviruses infecting cyanobacteria were found, except for a single high-light-inducible (hli) gene in S-CBS2 (24).…”