Chromid transforms opportunistic pathogen into beneficial symbiont to raise coral's thermal tipping point

Abstract

Resilient turbid coral reefs, found 1{degrees} north of the equator, experience fewer and less intense bleaching events despite being situated within the world's busiest shipping port in highly urbanised Singapore. We hypothesised that bacteria within the coral holobiont play a role in maintaining coral health by conferring traits that enhance thermal tolerance. Eleven Pseudovibrio isolates were obtained from the scleractinian coral Pachyseris speciosa, and their genomes differed by only four single nucleotide polymorphisms. A ~490 kbp chromid, pCJH, was present in 7 of the 11 isolates. A Pseudovibrio isolate without pCJH is an opportunistic pathogen of P. speciosa, accelerating bleaching disease. In contrast, the chromid reduces Pseudovibrio's fecundity, enhances its host colonisation and consequently increases P. speciosa's thermal tolerance by 1 {degrees}C. Interaction analyses in experimentally heat-stressed corals revealed a negative interaction between Pseudovibrio and Vibrio ASVs. The Pseudovibrio genomes and chromid encode several diffusible antibiotic biosynthetic gene clusters and two type six secretion systems (T6SS) for contact-dependent inhibition, with both types of inhibitory activity shown against opportunistic coral pathogens from local (i.e. isolated from the same coral host) and type-strain Vibrio spp. Together, these findings support the Coral Probiotic Hypothesis that bacteria enhance coral resilience, and identify a chromid responsible for Pseudovibrio's climatically driven Jekyll-and-Hyde lifestyle from opportunistic pathogen to beneficial symbiont.