Photosystem I gene cassettes are present in marine virus genomes

Like plant chloroplasts, the photosynthetic membranes of marine cyanobacteria contain two photosystems: photosystem II (PSII) mediates electron transfer from water to plastoquinones and PSI mediates electron transfer from plastocyanin to ferredoxin, thereby generating reducing power needed for CO2 fixation in the form of NADPH. Core PSII genes were recently found in cyanophages, viruses that infect cyanobacteria, where they presumably supplement the host's photosynthetic abilities. Now a trawl through metagenomic data from the Sorcerer II Global Ocean Sampling Expedition and through viral biomes reveals that PSI components are also present in cyanophages, presumably also contributing to overall photosynthetic performance. Cyanobacteria are important contributors to photosynthetic productivity in the open oceans. Functional photosystem II components are known to be encoded in cyanophage genomes and are suggested to provide a fitness advantage to the virus by boosting host performance. It is now shown that photosystem I components can also be detected in cyanophages. Cyanobacteria of the Synechococcus and Prochlorococcus genera are important contributors to photosynthetic productivity in the open oceans1,2,3. Recently, core photosystem II (PSII) genes were identified in cyanophages and proposed to function in photosynthesis and in increasing viral fitness by supplementing the host production of these proteins4,5,6,7. Here we show evidence for the presence of photosystem I (PSI) genes in the genomes of viruses that infect these marine cyanobacteria, using pre-existing metagenomic data from the global ocean sampling expedition8 as well as from viral biomes9. The seven cyanobacterial core PSI genes identified in this study, psaA, B, C, D, E, K and a unique J and F fusion, form a cluster in cyanophage genomes, suggestive of selection for a distinct function in the virus life cycle. The existence of this PSI cluster was confirmed with overlapping and long polymerase chain reaction on environmental DNA from the Northern Line Islands. Potentially, the seven proteins encoded by the viral genes are sufficient to form an intact monomeric PSI complex. Projection of viral predicted peptides on the cyanobacterial PSI crystal structure10 suggested that the viral–PSI components might provide a unique way of funnelling reducing power from respiratory and other electron transfer chains to the PSI.