Discovery of Euryhaline Phycoerythrobilin-Containing Synechococcus and Its Mechanisms for Adaptation to Estuarine Environments

Abstract

Understanding the strategies developed by different microbial groups to adapt to specific niches is critical. Through genome and transcriptome analyses of two newly isolated novel euryhaline Synechococcus strains, this study revealed that cluster 5 phycoerythrobilin-containing Synechococcus , which are thought to be strictly marine strains, could be abundant in low-salinity waters of the Pearl River estuary (salinity <15 ppt) and explained the molecular mechanisms that enabled them to adapt the low and fluctuating salinity in the estuarine environment. Synechococcus are among the most abundant and widely distributed picocyanobacteria on earth. Cluster 5 phycoerythrobilin-containing (PEB-containing) Synechococcus , the major marine Synechococcus , were considered to prefer high salinity, and they are absent in estuarine ecosystems. However, we have detected PEB-containing Synechococcus in some low-salinity (<15-ppt) areas of the Pearl River estuary at an abundance up to 1.0 × 10 5 cells ml −1 . Two PEB-containing Synechococcus strains (HK01 and LTW-R) were isolated, and tests on them revealed their ability to cope with variations in the salinity (from 14 to 44 ppt). Phylogenetic analysis showed that HK01 belonged to a novel Synechococcus clade (HK1), whereas LTW-R was clustered with S5.2 strains. Whole-genome analysis revealed that a membrane channel protein with glycine zipper motifs is unique to euryhaline Synechococcus . The upregulation of this protein, the osmotic sensors, and the heat shock protein HSP20 and the downregulation of the osmolyte biosynthesis enable euryhaline Synechococcus to well adapt to the low and fluctuating salinity in the estuarine environment. In addition, decreasing the salinity in LTW-R strongly downregulated several important metabolic pathways, including photosynthesis, and the Calvin-Benson cycle, whereas its growth was not significantly affected. Moreover, obtaining PEB genes from horizontal gene transfer expands the light niche significantly for euryhaline Synechococcus . These results provided new insights into the life strategies and ecological function of marine PEB-containing Synechococcus under the unique environmental condition of estuarine waters, particularly in response to salinity variations. IMPORTANCE Understanding the strategies developed by different microbial groups to adapt to specific niches is critical. Through genome and transcriptome analyses of two newly isolated novel euryhaline Synechococcus strains, this study revealed that cluster 5 phycoerythrobilin-containing Synechococcus , which are thought to be strictly marine strains, could be abundant in low-salinity waters of the Pearl River estuary (salinity <15 ppt) and explained the molecular mechanisms that enabled them to adapt the low and fluctuating salinity in the estuarine environment. This study expands current understanding on mechanisms involved in niche separation of marine Synechococcus lineages.