Osmotic stress response of the coral and oyster pathogenVibrio coralliilyticus: acquisition of catabolism gene clusters for the compatible solute and signaling moleculemyo-inositol

Abstract

Marine bacteria experience fluctuations in osmolarity that they must adapt to, and most bacteria respond to high osmolarity by accumulating compatible solutes. The osmotic stress response and compatible solutes used by the marine pathogen Vibrio coralliilyticus are unknown. In this study, we showed that to alleviate osmotic stress V. coralliilyticus biosynthesized the compatible solute glycine betaine (GB) and transported choline, GB, ectoine, dimethylglycine, and dimethylsulfoniopropionate, for osmoprotection, but not myo-inositol. Myo-inositol is a stress protectant and a signaling molecule that is biosynthesized by algae. Bioinformatics analysis identified two contiguous myo-inositol metabolic gene clusters in all V. coralliilyticus genomes. Growth pattern analysis demonstrated that V. coralliilyticus utilized myo-inositol as a sole carbon source, with a short 3 h lag time, and the inositol 2-dehydrogenase (iolG) gene was required for this growth. Genetic analysis identified both an MFS-type (IolT1) and ABC-type (IolXYZ) transporter in the metabolic gene clusters that transported myo-inositol. Further genomics and phylogenetic analyses showed that the myo-inositol metabolic gene clusters were widespread among Vibrionaceae (Vibrio, Photobacterium, Enterovibrio, and Grimontia species) and acquired several times within the group. IolG was most closely related to IolG from Aeromonas, Pectobacterium (formerly Erwinia), and Dickeya species. These species contained the iol genes in a single metabolic gene cluster with an iolXYZ transporter. In Aeromonas, the cluster was always found within mobile genetic elements, but present only in a few species, predominantly in strains of A. hydrophila and A. dhakensis.