The coral pathogenVibrio coralliilyticusutilizes the compatible solute and signaling moleculemyo-inositol as a sole carbon source

Abstract

AbstractMarine 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 pathogenVibrio coralliilyticusare unknown. In this study, we showed that to alleviate osmotic stressV. coralliilyticusbiosynthesized the compatible solute glycine betaine (GB) and transported choline, GB, ectoine, dimethylglycine, and dimethylsulfoniopropionate, for osmoprotection, but notmyo-inositol.Myo-inositol is a stress protectant and a signaling molecule that is biosynthesized by algae. Bioinformatics analysis identified two contiguousmyo-inositol metabolic gene clusters in allV. coralliilyticusgenomes. Growth pattern analysis demonstrated thatV. coralliilyticusutilizedmyo-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 transportedmyo-inositol. Further genomics and phylogenetic analyses showed that themyo-inositol metabolic gene clusters were widespread amongVibrionaceae(Vibrio, Photobacterium, Enterovibrio,andGrimontiaspecies) and acquired several times within the group. IolG was most closely related to IolG fromAeromonas, Pectobacterium (formerlyErwinia),andDickeyaspecies. These species contained theiolgenes in a single metabolic gene cluster with aniolXYZtransporter. InAeromonas, the cluster was always found within mobile genetic elements, but present only in a few species, predominantly in strains ofA. hydrophilaandA. dhakensis.ImportanceBacterial pathogens such asV. coralliilyticusencounter competition for nutrient sources and have evolved metabolic strategies to adapt to nutrient opportunities. Emerging studies show thatmyo-inositol is exchanged in the coral-algae symbiosis, likely involved in signaling, but is also a compatible solute in algae. Our findings that the coral pathogensV. coralliilyticusandV. mediterraneicontainedmyo-inositol metabolism gene clusters suggest this could be an important adaptation. The consumption ofmyo-inositol by these coral pathogens could contribute to a breakdown of the coral-algae symbiosis by inhibition of algal survival or algal expulsion leading to coral bleaching. Phylogenetic analysis showed that amyo-inositol metabolism gene cluster is ancestral toPectobacteriumandDickeya, but was acquired recently by horizontal gene transfer in hypervirulent strains ofAeromonas.