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 also known as osmolytes. The osmotic stress response and compatible solutes used by the coral and oyster pathogenVibrio coralliilyticuswere unknown. In this study, we showed that to alleviate osmotic stressV. coralliilyticusbiosynthesized glycine betaine (GB) and transported into the cell choline, GB, ectoine, dimethylglycine, and dimethylsulfoniopropionate, but notmyo-inositol.Myo-inositol is a stress protectant and a signaling molecule that is biosynthesized and used by algae. Bioinformatics identifiedmyo-inositol (iol) catabolism clusters inV. coralliilyticusand otherVibrio, Photobacterium, Grimontia,andEnterovibriospecies. Growth pattern analysis demonstrated thatV. coralliilyticusutilizedmyo-inositol as a sole carbon source, with a short lag time of 3 h. AniolGdeletion mutant, which encodes an inositol dehydrogenase, was unable to grow onmyo-inositol. Within theiolclusters were an MFS-type (iolT1)and an ABC-type (iolXYZ)transporter and analyses showed that both transportedmyo-inositol. IolG and IolA phylogeny amongVibrionaceaespecies showed different evolutionary histories indicating multiple acquisition events. Outside ofVibrionaceae, IolG was most closely related to IolG from a small group ofAeromonasfish and human pathogens andProvidenciaspecies. However, IolG from hypervirulentA. hydrophilastrains clustered with IolG fromEnterobacter,and divergently fromPectobacterium, Brenneria,andDickeyaplant pathogens. Theiolcluster was also present withinAliiroseovarius, Burkholderia, Endozoicomonas, Halomonas, Labrenzia, Marinomonas, Marinobacterium, Cobetia, Pantoea,andPseudomonas,of which many species were associated with marine flora and fauna.IMPORTANCEHost associated bacteria such asV. coralliilyticusencounter competition for nutrients and have evolved metabolic strategies to better compete for food. Emerging studies show thatmyo-inositol is exchanged in the coral-algae symbiosis, is likely involved in signaling, but is also an osmolyte in algae. The bacterial consumption ofmyo-inositol could contribute to a breakdown of the coral-algae symbiosis during thermal stress or disrupt the coral microbiome. Phylogenetic analyses showed that the evolutionary history ofmyo-inositol metabolism is complex, acquired multiple times inVibrio,but acquired once in many bacterial plant pathogens. Further analysis also showed that a conservediolcluster is prevalent among many marine species (commensals, mutualists, and pathogens) associated with marine flora and fauna, algae, sponges, corals, molluscs, crustaceans, and fish.