A beneficial megaplasmid transforms an opportunistic bacterial pathogen to benefit coral by extending their thermal range

Abstract Resilient turbid coral reefs, found 1° 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 diversity within this extreme environment by conferring traits that enhance host tolerance. Eleven Pseudovibrio isolates, whose genomes differ by only four SNPs, were isolated from the scleractinian coral Pachyseris speciosa . A ∼490 kbp megaplasmid (pCJH) was found in 7 of the 11 Pseudovibrio isolates. This study identified an opportunistic Pseudovibrio sp. pathogen of P. speciosa , accelerating bleaching disease. However, presence of the megaplasmid alters the ecological strategy of Pseudovibrio sp. toward mutualism, delaying coral bleaching. The megaplasmid enhances Pseudovibrio’ s host colonisation and establishment of symbiosis through increased attachment and extends its bioactive genetic potential, but reduces fecundity. The Pseudovibrio genomes and megaplasmid encode several diffusible antibiotic biosynthetic gene clusters and contact-dependent inhibition mechanisms, with both types of inhibitory activity shown against local (i.e. P. speciosa ) and type-strain Vibrio spp. Interaction analyses in experimentally heat-stressed corals revealed negative associations between Pseudovibrio and Vibrio ASVs corresponding to these cultured isolates. They also showed increased coral thermal tolerance by a full degree (1°C) when it is associated with the megaplasmid-bearing strain. Together, these findings support the Coral Probiotic Hypothesis that bacteria enhance coral resilience through chemical defense and identifies additional aspects to this symbiosis by a mobile genetic element which could play an important role in coral reef resilience.