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...

The discovery of the genes psbA and psbD, encoding the D1 and D2 core components of the photosynthetic reaction center PSII (photosystem II), in the genome of the bacteriophage S-PM2 (a cyanomyovirus) that infects marine cyanobacteria begs the question as to how these genes were acquired. In an attempt to answer this question, it was established that the occurrence of the genes is widespread among marine cyanomyovirus isolates and may even extend to podoviruses. The phage psbA genes fall into a clade that includes the psbA genes from their potential Synechococcus and Prochlorococcus hosts, and thus, this phylogenetic analysis provides evidence to support the idea of the acquisition of these genes by horizontal gene transfer from their cyanobacterial hosts. However, the phage psbA genes form distinct subclades within this lineage, which suggests that their acquisition was not very recent. The psbA genes of two phages contain identical 212-bp insertions that exhibit all of the canonical structural features of a group I self-splicing intron. The different patterns of genetic organization of the psbAD region are consistent with the idea that the psbA and psbD genes were acquired more than once by cyanomyoviruses and that their horizontal transfer between phages via a common phage gene pool, as part of mobile genetic modules, may be a continuing process. In addition, genes were discovered encoding a high-light inducible protein and a putative key enzyme of dark metabolism, transaldolase, extending the areas of host-cell metabolism that may be affected by phage infection. Strains of unicellular cyanobacteria Synechococcus and Prochlorococcus are abundant in the world's oceans, and they dominate the prokaryotic component of the picophytoplankton. Together, they contribute 32-89% of primary production in oligotrophic regions of the oceans (1-4). The recent discovery (5) that a phage infecting marine Synechococcus strains encodes key photosynthetic genes has important implications for our understanding of the effect of phage infection on the photosynthetic picophytoplankton physiology and consequent impact on major biogeochemical cycles. The acquisition of photosynthesis genes by a phage, presumably by horizontal gene transfer, begs the questions of (i) how common the possession of photosynthesis genes by such phages is, (ii) where the acquired genes were from, and (iii) whether the acquisition was a single rare ancestral event or a common phenomenon in the oceans.The cyanobacterial picoplankton, together with all organisms capable of oxygenic photosynthesis, possess two photosynthetic reaction centers, PSI and PSII (photosystems I and II). The PSII complex is a large protein-pigment assembly in the thylakoid membrane that catalyses the light-dependent oxidation of water to molecular oxygen. At the core of PSII lies a heterodimer of two related proteins, D1 and D2, which binds the pigments and cofactors necessary for primary photochemistry. During active photosynthesis, D1 and, to a lesser extent, D2 turn over rapidly as...