The Genome of S-PM2, a “Photosynthetic” T4-Type Bacteriophage That Infects Marine Synechococcus Strains

Abstract

Bacteriophage S-PM2 infects several strains of the abundant and ecologically important marine cyanobacterium Synechococcus. A large lytic phage with an isometric icosahedral head, S-PM2 has a contractile tail and by this criterion is classified as a myovirus ( Strains of unicellular cyanobacteria of the genera Synechococcus and Prochlorococcus are abundant in the world's oceans and constitute the prokaryotic component of the picophytoplankton. Together, these photosynthetic bacteria contribute a significant proportion of primary production in oligotrophic regions of the oceans (21,35,37,68). Viral infection of marine unicellular cyanobacteria was first reported in 1990 (53, 63), and cyanovirus isolates were first characterized in the laboratory in 1993 (62,69,74). The majority of these phages belong to the myoviruses. Myoviruses are physically robust and remarkably versatile; this virion design can apparently be easily adapted to a variety of different ecological niches (64). S-PM2 is a lytic cyanomyovirus with an icosahedral head and long contractile tail that infects marine Synechococcus strains. The genome has been shown to have a size of ϳ194 kb (27). Bacteriophage T4 that infects Escherichia coli is the archetype myovirus, and S-PM2 was shown to have a genetic module that encodes distant homologues of most of the major virion proteins of T4 (27). T4 has been extensively studied and is extremely well understood; it serves as a superb, if somewhat complex, model for S-PM2.A previous phylogenetic analysis of the sequences of the major head and tail genes of a wide range of T4-type bacteriophages indicated at least three distinct phylogenetic subgroups of these phages (64). There is a large cluster of phages, termed the T-evens, members of which are all closely related to T4, the archetype of the Myoviridae. The second subgroup is surprisingly phylogenetically divergent from the T-evens, but morphologically similar; these are called the pseudoT-evens (47), and they includes phages such as RB49 and RB42 that infect E. coli. The third cluster includes Aeromonas phages and vibriophages such as nt-1, KVP20, KVP40, 65, and Aeh1. Such phages have heads that are more elongated than those of both T-evens and the pseudoT-evens and thus are called the schizoT-evens (64). Phylogenetic analysis based on the major capsid protein gp23 has shown that S-PM2 and the related cyanomyovirus S-PWM3 are quite distinct from the other characterized T4-like phages and form a new discrete group, the exoT-evens (27). These marine T4-type phages have apparently diverged significantly from the T4 archetype. Beyond the fact that they have a contractile tail, these phages have little morphological resemblance to the other T4-type phages. Among the many differences between the exoT-evens and the other T-type phages are those that relate to the photosynthetic physiology of their hosts. It is clear that S-PM2 (41) and several other marine cyanomyoviruses (36, 43) encode homologues of the D1 and D2 proteins of the host photosystem II that presum...

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

“…Cyanophages, viruses that infect cyanobacteria, are abundant and broadly distributed in the global oceans (Suttle, 2007;Williamson et al, 2008). Cyanophage genomes carry orthologs of host genes involved in a variety of host processes, including phosphate acquisition, carbon metabolism, photosynthesis and response to light stress (Lindell et al, 2004;Mann et al, 2005;Sullivan et al, 2005;Weigele et al, 2007;Sullivan et al, 2010).…”

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).…”

“…(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.…”

Viral photosynthetic reaction center genes and transcripts in the marine environment

“…The D1 and D2 proteins form the reaction center dimer of PSII that binds the primary electron donors and acceptors. Oxygenic photosynthesis genes were recently found in the genomes of cyanophages from two different viral families (Myoviridae and Podoviridae) (Mann et al, 2003(Mann et al, , 2005Lindell et al, 2004;Millard et al, 2004;Sullivan et al, 2005). A variety of viral photosynthesis genes were identified: for example, psbA, encoding the D1 protein; psbD, encoding the D2 protein; hli genes, encoding the HLIPs (high-light inducible proteins); and the petE and petF genes, encoding the photosynthetic electron transport proteins plastocyanin and ferredoxin, respectively (for recent review, see Clokie and Mann, 2006).…”