A novel salt-tolerant genotype illuminates the sucrose gene evolution in freshwater bloom-forming cyanobacterium Microcystis aeruginosa

Microcystis aeruginosa is a water bloom-forming cyanobacterium found in fresh and brackish water ecosystems worldwide. Previously, we showed that several instances of M. aeruginosa bloom in brackish water can be explained by the proliferation of salt-tolerant M. aeruginosa strains harboring genes for a compatible solute sucrose. However, evolutionary history of sucrose genes in M. aeruginosa remains unclear because salt-tolerant strains have been poorly described. Here, we characterized a novel salt-tolerant strain of M. aeruginosa (NIES-4325) isolated from the brackish water of Lake Abashiri, Japan. A whole-genome analysis of M. aeruginosa NIES-4325 identified genes for sucrose synthesis (sppA, spsA and susA). Quantitative sucrose and gene expression analyses suggested that sucrose is implicated in acclimation to high salt in NIES-4325. Notably, the sucrose genes of M. aeruginosa are monophyletic, yet sucrose genes of NIES-4325 are highly divergent from those of other salt-tolerant M. aeruginosa strains. This suggests an early sucrose gene import into M. aeruginosa from other cyanobacteria, followed by multiple losses during intraspecific diversification. One of a few survivors of salt-tolerant strains is a likely donor of recent horizontal spreads of sucrose genes across M. aeruginosa lineages.