Among the wealth of microbial organisms inhabiting marine environments, cyanobacteria (blue-green algae) are the most abundant photosynthetic cells.
Prochlorococcus and
Synechococcus, the two most common cyanobacteria, account for 30% of global carbon fixation (through the photosynthetic process in which sugars are manufactured from carbon dioxide and water). By drawing on natural resources, these microbes use photosystems (PS) I and II (the two reaction centers in
photosynthesis) to harness energy.
Intriguingly, some viruses that infect cyanobacteria (called cyanophage), carry
genes that encode two PSII core reaction-center proteins: PsbA (the most rapidly turned over core protein in all oxygen-yielding photosynthetic organisms) and PsbD (which forms a complex with PsbA). By expressing their own copies of
psbA and
psbD during infection, these
cyanophages have managed to co-opt host genes to suit their own purposes: enhancing photosynthesis. It seems likely that they do this in the interests of their own fitness, since
cyanophage production is optimal when photosynthesis is maintained during infection.
Until recently, only a small sample of cyanophages had been examined, leaving open the questions of how widespread PSII genes are in these organisms and where the genes came from. To answer these questions, Matthew Sullivan, Debbie Lindell, Sallie Chisholm, and colleagues examined a pool of 33 cyanophage isolates (cultured from samples collected from the Sargasso Sea and the Red Sea), along with data already available for nine other cyanophages, for the presence of
psbA and
psbD genes. They found
psbA was present in 88% and
psbD in 50% of the cyanophages studied. By analyzing the sequences of these genes along with those from
Prochlorococcus and
Synechococcus host genes, they reconstructed the evolutionary history of how the PSII genes entered the phage genomes.
Cyanophages are divided morphologically into three main families (Podoviridae, Myoviridae, and Siphoviridae). Looking at the distributions of the PSII genes across the different families, Sullivan, Lindell, et al. saw that
psbA was present in all
myoviruses and all
Prochlorococcus podoviruses, but not in
Prochlorococcus siphoviruses or
Synechococcus podoviruses. The high levels of sequence conservation between the different cyanophages suggest that this gene is probably functional and that it is likely to increase the reproductive fitness of the phage. The length of the latent period may impact the distribution pattern of
psbA among these phage groups. However, more information about the physiological characteristics of cyanophages is needed to further investigate these possibilities.
The second gene,
psbD, was less prolific but was seen in four of the 20
Prochlorococcus myoviruses and 17 of the 20
Synechococcus myoviruses examinedall of which also encoded
psbA. Myoviruses are known to infect a wider range of cyanobacteria than the other cyanophage families. Indeed, when investigated, the
psbD-encoding myoviruses correlated with those known to have a broader host range. Perhaps the co-opting of both PSII genes ensures a functional PsbAPsbD protein complex to enhance infection for these cyanophages that are able to infect a wider range of hosts.
To determine when the PSII genes had been transferred into the phage and from where, Sullivan, Lindell, et al. investigated the nucleotide sequences of
psbA and
psbD from both
Prochlorococcus and
Synechococcus host and cyanophage. Using meticulous sequence analyses and standard statistical methods, they generated phylogenetic trees to explain the evolutionary history of these two PSII genes.
By analyzing the clusters of sequence types within the resulting tree, the authors saw evidence that
psbA was transferred from th