Virulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens

The increase in prevalence and severity of coral disease outbreaks produced by Vibrio pathogens, and related to global warming, has seriously impacted reef-building corals throughout the oceans. The coral Oculina patagonica has been used as a model system to study coral bleaching produced by Vibrio infection. Previous data demonstrated that when two coral pathogens (Vibrio coralliilyticus and Vibrio mediterranei) simultaneously infected the coral O. patagonica, their pathogenicity was greater than when each bacterium was infected separately. Here, to understand the mechanisms underlying this synergistic effect, transcriptomic analyses of monocultures and cocultures as well as experimental infection experiments were performed. Our results revealed that the interaction between the two vibrios under culture conditions overexpressed virulence factor genes (e.g., those encoding siderophores, the type VI secretion system, and toxins, among others). Moreover, under these conditions, vibrios were also more likely to form biofilms or become motile through induction of lateral flagella. All these changes that occur as a physiological response to the presence of a competing species could favor the colonization of the host when they are present in a mixed population. Additionally, during coral experimental infections, we showed that exposure of corals to molecules released during V. coralliilyticus and V. mediterranei coculture induced changes in the coral microbiome that favored damage to coral tissue and increased the production of lyso-platelet activating factor. Therefore, we propose that competition sensing, defined as the physiological response to detection of harm or to the presence of a competing Vibrio species, enhances the ability of Vibrio coral pathogens to invade their host and cause tissue necrosis.IMPORTANCEVibrio coralliilyticus and Vibrio mediterranei are important coral pathogens capable of inducing serious coral damage, which increases severely when they infect the host simultaneously. This has consequences related to the dispersion of these pathogens among different locations that could enhance deleterious effects on coral reefs. However, the mechanisms underlying this synergistic interaction are unknown. The work described here provides a new perspective on the complex interactions among these two Vibrio coral pathogens, suggesting that coral infection could be a collateral effect of interspecific competition. Major implications of this work are that (i) Vibrio virulence mechanisms are activated in the absence of the host as a response to interspecific competition and (ii) release of molecules by Vibrio coral pathogens produces changes in the coral microbiome that favor the pathogenic potential of the entire Vibrio community. Thus, our results highlight that social cues and competition sensing are crucial determinants of development of coral diseases.