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.

Marine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS). While light and ROS could act synergistically on the impairment of photosynthesis, inducing photodamage and inhibiting photosystem II repair, acclimation to high irradiance is also thought to confer resistance to other stressors. To identify the respective roles of light and ROS in the photoinhibition process and detect a possible light-driven tolerance to oxidative stress, we compared the photophysiological and transcriptomic responses of Synechococcus sp. WH7803 acclimated to low light (LL) or high light (HL) to oxidative stress, induced by hydrogen peroxide (H 2 O 2 ) or methylviologen. While photosynthetic activity was much more affected in HL than in LL cells, only HL cells were able to recover growth and photosynthesis after the addition of 25 mM H 2 O 2 . Depending upon light conditions and H 2 O 2 concentration, the latter oxidizing agent induced photosystem II inactivation through both direct damage to the reaction centers and inhibition of its repair cycle. Although the global transcriptome response appeared similar in LL and HL cells, some processes were specifically induced in HL cells that seemingly helped them withstand oxidative stress, including enhancement of photoprotection and ROS detoxification, repair of ROS-driven damage, and regulation of redox state. Detection of putative LexA binding sites allowed the identification of the putative LexA regulon, which was downregulated in HL compared with LL cells but up-regulated by oxidative stress under both growth irradiances.