The dominant marine Synechococcus clade II exhibits a non-canonical transcriptional response to cope with thermal stress

Temperature significantly impacts the growth and distribution of marine cyanobacteria, which employ diverse strategies to cope with temperature variations. However, the molecular mechanisms underlying thermal acclimation in cyanobacterial taxa that dominate vast oligotrophic regions of the ocean, such as the Synechococcus clade II, remain unknown. Here, we analysed the physiological and global transcriptional response of an ecologically relevant clade II strain (Synechococcus sp. RS9907) to long-term thermal acclimation at temperatures from 20 to 33 °C. The growth rate in RS9907 increased linearly with temperature up to the warm threshold (33 °C), but genes related with the heat-shock response were upregulated within the range of 28 to 33 °C, indicating significant cellular stress under warm conditions. Carbon fixation and assimilation genes (rcbLS, cbbA, zwf, glgP) showed minimum expression values at 20 °C and 33 °C, but the diel expression patterns of these genes remained unaffected by temperature conditions, being consistently upregulated during day-time. By contrast, some genes involved in photosynthesis (acpA, psbABO, psaABD) were strongly upregulated during night-time under warm conditions, suggesting regulatory imbalances during the diel cycle. Notably, the expression of genes related to the synthesis of osmolytes against salt stress and fatty acid desaturases, which are typically upregulated under cold temperature in other cyanobacteria, was induced in warm acclimated RS9907 cells. These results highlight distinct transcriptional mechanisms of thermal acclimation in members of the Synechococcus clade II compared to other cyanobacterial lineages. This emphasizes the importance of understanding the diverse and intricate ways in which marine cyanobacteria adapt to temperature fluctuations.