Sucrose in bloom‐forming cyanobacteria: loss and gain of genes involved in its biosynthesis

<jats:title>Summary</jats:title><jats:p>Bloom‐forming cyanobacteria are widely distributed in freshwater ecosystems. To cope with salinity fluctuations, cyanobacteria synthesize compatible solutes, such as sucrose, to maintain the intracellular osmotic balance. The screening of cyanobacterial genomes revealed that homologues to sucrose metabolism‐related genes only occur in few bloom‐forming strains, mostly belonging to <jats:styled-content style="fixed-case">N</jats:styled-content>ostocales and <jats:styled-content style="fixed-case">S</jats:styled-content>tigonematales orders. Remarkably, among <jats:styled-content style="fixed-case">C</jats:styled-content>hroococcales and <jats:styled-content style="fixed-case">O</jats:styled-content>scillatoriales strains, homologues were only found in <jats:styled-content style="fixed-case"><jats:italic>M</jats:italic></jats:styled-content><jats:italic>. aeruginosa</jats:italic> <jats:styled-content style="fixed-case">PCC</jats:styled-content> 7806 and <jats:styled-content style="fixed-case"><jats:italic>L</jats:italic></jats:styled-content><jats:italic>eptolyngbya boryana</jats:italic> <jats:styled-content style="fixed-case">PCC</jats:styled-content> 6306, suggesting a massive loss of sucrose metabolism in bloom‐forming strains of these orders. After a complete functional characterization of sucrose genes in <jats:styled-content style="fixed-case"><jats:italic>M</jats:italic></jats:styled-content><jats:italic>. aeruginosa</jats:italic> <jats:styled-content style="fixed-case">PCC</jats:styled-content> 7806, we showed that sucrose metabolism depends on the expression of a gene cluster that defines a transcriptional unit, unique among all sucrose‐containing cyanobacteria. It was also demonstrated that the expression of the encoding genes of sucrose‐related proteins is stimulated by salt. In view of its ancestral origin in cyanobacteria, the fact that most bloom‐forming strains lack sucrose metabolism indicates that the genes involved might have been lost during evolution. However, in a particular strain, like <jats:styled-content style="fixed-case"><jats:italic>M</jats:italic></jats:styled-content><jats:italic>. aeruginosa</jats:italic> <jats:styled-content style="fixed-case">PCC</jats:styled-content> 7806, sucrose synthesis genes were probably regained by horizontal gene transfer, which could be hypothesized as a response to salinity fluctuations.</jats:p>