Genomic and Transcriptomic Insights into Salinity Tolerance-Based Niche Differentiation of Synechococcus Clades in Estuarine and Coastal Waters

Cluster 5 Synechococcus is one of the most important primary producers on earth. However, ecotypes of this genus exhibit complex geographical distributions, and the genetic basis of niche partitioning is still not fully understood. Here, we report distinct distributions of subcluster 5.1 (SC5.1) and subcluster 5.2 (SC5.2) Synechococcus in estuarine waters, and we reveal that salinity is the main factor determining their distribution. Clade III (belonging to SC5.1) and CB4 (belonging to SC5.2) are dominant clades in the study region, with different ecological distributions. We further conducted physiological, genomic, and transcriptomic studies of Synechococcus strains YX04-3 and HK05, which are affiliated with clade III and CB4, respectively. Laboratory tests showed that HK05 could grow at low salinity (13 ppt), whereas the growth of YX04-3 was suppressed when salinity decreased to 13 ppt. Genomic and transcriptomic analysis suggested that euryhaline clade CB4 is capable of dealing with a sudden drop of salinity by releasing compatible solutes through mechanosensitive channels that are coded by the mscL gene, decreasing biosynthesis of organic osmolytes, and increasing expression of heat shock proteins and high light-inducible proteins to protect photosystem. Furthermore, CB4 strain HK05 exhibited a higher growth rate when growing at low salinity than at high salinity. This is likely achieved by reducing its biosynthesis of organic osmolyte activity and increasing its photosynthetic activity at low salinity, which allowed it to enhance the assimilation of inorganic carbon and nitrogen. Together, these results provide new insights regarding the ecological distribution of SC5.2 and SC5.1 ecotypes and their underlying molecular mechanisms. IMPORTANCE Synechococcus is a group of unicellular Cyanobacteria that are widely distributed in global aquatic ecosystems. Salinity is a factor that affects the distribution of microorganisms in estuarine and coastal environments. In this study, we studied the distribution pattern of Synechococcus community along the salinity gradient in a subtropical estuary. By using omic methods, we unveiled genetic traits that determine the niche partitioning of euryhaline and strictly marine Synechococcus. We also explored the strategies employed by euryhaline Synechococcus to cope with a sudden drop of salinity, and revealed possible mechanisms for the higher growth rate of euryhaline Synechococcus in low salinity conditions. This study provides new insight into the genetic basis of niche partitioning of Synechococcus clades.