Osmotic stress response of the coral and oyster pathogen Vibrio coralliilyticus: acquisition of catabolism gene clusters for the compatible solute and signal molecule myo-inositol

Authors: BOAS LICHTY, KATHERINE, E. - University Of Delaware; LOUGHRAN, RACHEL - University Of Delaware; USHIJIMA, BLAKE - University Of North Carolina-Wilmington; Richards, Gary; BOYD, FIDELMA - University Of Delaware

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/22/2024
Publication Date: 6/14/2024
Citation: Boas Lichty, K., Loughran, R.M., Ushijima, B., Richards, G.P., Boyd, F. 2024. Osmotic stress response of the coral and oyster pathogen Vibrio coralliilyticus: acquisition of catabolism gene clusters for the compatible solute and signal molecule myo-inositol. Applied and Environmental Microbiology. https://doi.org/10.1128/aem.00920-24.
DOI: https://doi.org/10.1128/aem.00920-24

Interpretive Summary: Vibrio coralliilyticus is a marine bacterium that is pathogenic to corals and larval oysters. Coral survival is dependent on the presence of a symbiotic relationship with marine algae. These algae produce a stress protectant and signaling molecule known as myo-inositol, a sugar which protects the algae against osmotic stress. Emerging studies show that myo-inositol is exchanged in the algae-coral symbiosis and helps regulate osmotic pressure in the cell. The consumption of myo-inositol by V. coralliilyticus could contribute to a breakdown of the coral-algal symbiosis during periods of thermal stress. We demonstrated that V. coralliilyticus can grow on myo-inositol as the sole carbon source. In V. coralliilyticus, two distinct clusters of genes responsible for the regulation, transport, and breakdown of myo-inositol were identified and are described. Phylogenetic analyses showed that the evolutionary history of myo-inositol metabolism is complex. Analyses showed that a myo-inositol gene cluster is prevalent among many marine species associated with marine flora and fauna, algae, sponges, corals, molluscs, crustaceans, and fish.

Technical 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 pathogen Vibrio coralliilyticus were unknown. In this study, we showed that to alleviate osmotic stress V. coralliilyticus biosynthesized glycine betaine (GB) and transported into the cell choline, GB, ectoine, dimethylglycine, and dimethylsulfoniopropionate, but not myo-inositol. Myo-inositol is a stress protectant and a signaling molecule that is biosynthesized and used by algae. Bioinformatics identified myo-inositol (iol) catabolism clusters in V. coralliilyticus and other Vibrio, Photobacterium, Grimontia, and Enterovibrio species. Growth pattern analysis demonstrated that V. coralliilyticus utilized myo-inositol as a sole carbon source, with a short lag time of 3 h. An iolG deletion mutant, which encodes an inositol dehydrogenase, was unable to grow on myo-inositol. Within the iol clusters were an MFS-type (iolT1) and an ABC-type (iolXYZ) transporter and analyses showed that both transported myo-inositol. IolG and IolA phylogeny among Vibrionaceae species showed the myo-inositol clusters had different evolutionary histories indicating multiple acquisition events. Outside of Vibrionaceae, IolG was most closely related to IolG from a small group of Aeromonas fish and human pathogens present as a single cluster within mobile genetic elements. IolG from hypervirulent A. hydrophila strains clustered with IolG from Enterobacter, and Pectobacterium, Brenneria, and Dickeya plant pathogens. The iol cluster was also present within Aliiroseovarius, Burkholderia, Endozoicomonas, Halomonas, Labrenzia, Marinomonas, Marinobacterium, Cobetia, Pantoea, and Pseudomonas, of which many species were associated with marine flora and fauna.