There is growing recognition that the health of animals and plants depends, to some extent, on their microbiome. Although disease risk has long been linked to environmental factors such as temperature that can control the reproductive success of pathogens or the immune response of plants and animals, much less is known about the role of the microbiome in thwarting outbreaks. We used the endangered Caribbean staghorn coral A. cervicornis as a model system to understand how the microbiome affects the spread of White Band Disease, a disease likely caused by a pathogenic bacterium. Specifically, we used a combination of manipulative experiments, field surveys and mathematical modeling to determine how the bacteria that make-up the coral microbiome can reduce disease risk by outcompeting invasive pathogenic bacteria.

Our experiment included three factors: antibiotic exposure (high levels of antibiotics vs. none), first dose (exposure to microbes from healthy vs. diseased corals) and second dose (exposure to microbes from healthy vs. diseased corals). We analyzed the response of corals and their microbiomes to these different treatment combinations in order to test three hypotheses: an antibiotic effect, a probiotic effect and a priority effect. 

Exposure to antibiotics reduced disease prevalence. Corals exposed to different antibiotic treatments were also characterized by strong and persistent differences in their microbial communities. Taken together, these results validated the antibiotic effect hypothesis by demonstrating that the antibiotic treatment had a positive influence on the health of corals, which adds to the body of evidence suggesting that White Band Disease is likely caused by a bacterial agent.

The probiotic effect was relatively weak but present. Corals that received a double dose of microbes from healthy corals had microbiomes that were more similar to those of corals that never received antibiotics than to those that did. Conversely, corals that received a double dose of microbes from diseased corals had microbiomes that were more similar to those of corals that received antibiotics. This suggests that the antibiotic treatment suppressed the natural microbiome found in healthy corals and thus promoted the ability of microbes from diseased corals to invade, whereas corals that received no antibiotics retained their natural microbiomes which resisted invasion from microbes contained in the exposure treatment. Hence, this points to a potentially antagonistic interaction between the probiotic effect and the antibiotic effect with respect to the stability of the coral microbiome.

Finally, there was no evidence of a priority effect because corals that were exposed to microbes from diseased corals first and healthy corals second had essentially the same microbiomes as the corals that were exposed to microbes from healthy corals first and diseased corals second. This means that microbes from healthy corals did not suppress the invasion of microbes from diseased corals simply by preempting space or resources in the coral. Hence, the outcome of microbial competition does not depend on initial conditions such as initial abundance and arrival order and is thus likely more predictable.

We then conducted a field experiment that examined two facets of stability, namely resistance and resilience, in the microbiomes of Caribbean corals using a perturbation consisting of a large dose of antibiotics to disrupt the host microbiome. We found that corals harbored species-specific microbiomes that persisted through time despite experimental antibiotic perturbation. Interestingly, the microbiomes of species that exhibited the greatest resistance and resilience to the experimental perturbation tended to be the least stable in co-located field surveys, which suggests that natural patterns of microbiome variability can be poor predictors of their response to perturbations. We used a mathematical model to help resolve this apparent paradox. Our model showed that the regulating effects of antibiotics on microbiomes depended on whether their production was associated with corals or their microbiomes. Specifically, we showed that microbial regulation could be described as a ?glass cannon? in that it mounts a potent attack on invading pathogens that depends on beneficial microbes that are themselves vulnerable to disruption.

Overall, this project has shown that the interactions between the microbiome and its host can have important implications for conserving and restoring coral species. For instance, the antagonistic interaction between the probiotic and the antibiotic effect suggests that applying antibiotics in nurseries as a prophylactic measure may be counterproductive and endanger the health of corals by preventing their natural microbiomes from resisting pathogenic microbes. Additionally, our results caution against using corals that exhibit high stability to seed restoration projects because they may be vulnerable to infection.

In terms of broader impacts, this project provided research training for two undergraduate students and six postgraduate students (3 M.Sc., 3 Ph.D.), as well as one postdoctoral scholar. To date, this award has also generated 21 peer reviewed publications or presentations at scientific meetings. Finally, the experimental data obtained as part of this project is available on our BCO-DMO project page (https://www.bco-dmo.org/project/541019).

Last Modified: 05/07/2020
Modified by: Tarik C Gouhier