Function and evolution of the psbA gene family in marine Synechococcus: Synechococcus sp. WH7803 as a case study

In cyanobacteria, the D1 protein of photosystem II (PSII) is encoded by the psbA multigene family. In most freshwater strains, a D1:1 isoform of this protein is exchanged for a D1:2 isoform in response to various stresses, thereby altering PSII photochemistry. To investigate PSII responses to stress in marine Synechococcus, we acclimated cultures of the WH7803 strain to different growth irradiances and then exposed them to high light (HL) or ultraviolet (UV) radiation. Measurement of PSII quantum yield and quantitation of the D1 protein pool showed that HL-acclimated cells were more resistant to UV light than were low light- (LL) or medium light- (ML) acclimated cells. Both UV and HL induced the expression of psbA genes encoding D1:2 and the repression of the psbA gene encoding D1:1. Although three psbA genes encode identical D1:2 isoforms in Synechococcus sp. WH7803, only one was strongly stress responsive in our treatment conditions. Examination of 11 marine Synechococcus genomic sequences identified up to six psbA copies per genome, with always a single gene encoding D1:1. In phylogenetic analyses, marine Synechococcus genes encoding D1:1 clustered together, while the genes encoding D1:2 grouped by genome into subclusters. Moreover, examination of the genomic environment of psbA genes suggests that the D1:2 genes are hotspots for DNA recombination. Collectively, our observations suggest that while all psbA genes follow a concerted evolution within each genome, D1:2 coding genes are subject to intragenome homogenization most probably mediated by gene conversion.