Marine <i>Synechococcus</i> picocyanobacteria: Light utilization across latitudes.

Abstract

The most ubiquitous cyanobacteria, <i>Synechococcus</i>, have colonized different marine thermal niches through the evolutionary specialization of lineages adapted to different ranges of temperature seawater. We used the strains of <i>Synechococcus</i> temperature ecotypes to study how light utilization has evolved in the function of temperature. The tropical <i>Synechococcus</i> (clade II) was unable to grow under 16 °C but, at temperatures >25 °C, induced very high growth rates that relied on a strong synthesis of the components of the photosynthetic machinery, leading to a large increase in photosystem cross-section and electron flux. By contrast, the <i>Synechococcus</i> adapted to subpolar habitats (clade I) grew more slowly but was able to cope with temperatures <10 °C. We show that growth at such temperatures was accompanied by a large increase of the photoprotection capacities using the orange carotenoid protein (OCP). Metagenomic analyzes revealed that <i>Synechococcus</i> natural communities show the highest prevalence of the <i>ocp</i> genes in low-temperature niches, whereas most tropical clade II <i>Synechococcus</i> have lost the gene. Moreover, bioinformatic analyzes suggested that the OCP variants of the two cold-adapted <i>Synechococcus</i> clades I and IV have undergone evolutionary convergence through the adaptation of the molecular flexibility. Our study points to an important role of temperature in the evolution of the OCP. We, furthermore, discuss the implications of the different metabolic cost of these physiological strategies on the competitiveness of <i>Synechococcus</i> in a warming ocean. This study can help improve the current hypotheses and models aimed at predicting the changes in ocean carbon fluxes in response to global warming.