Host–microbial systems as glass cannons: Explaining microbiome stability in corals exposed to extrinsic perturbations

Although stability is relatively well understood in macro-organisms, much less is known about its drivers in host-microbial systems where processes operating at multiple levels of biological organisation jointly regulate the microbiome. We conducted an experiment to examine the microbiome stability of three Caribbean corals (Acropora cervicornis, Pseudodiploria strigosa and Porites astreoides) by placing them in aquaria and exposing them to a pulse perturbation consisting of a large dose of broad-spectrum antibiotics before transplanting them into the field. We found that coral hosts harboured persistent, species-specific microbiomes. Stability was generally high but variable across coral species, with A. cervicornis microbiomes displaying the lowest community turnover in both the non-perturbed and the perturbed field transplants. Interestingly, the microbiome of P. astreoides was stable in the non-perturbed field transplants, but unstable in the perturbed field transplants. A mathematical model of host-microbial dynamics helped resolve this paradox by showing that when microbiome regulation is driven by host sanctioning, both resistance and resilience to invasion are low and can lead to instability despite the high direct costs bourne by corals. Conversely, when microbiome regulation is mainly associated with microbial processes, both resistance and resilience to invasion are high and promote stability at no direct cost to corals. We suggest that corals that are mainly regulated by microbial processes can be likened to 'glass cannons' because the high stability they exhibit in the field is due to their microbiome's potent suppression of invasive microbes. However, these corals are susceptible to destabilisation when exposed to perturbations that target the vulnerable members of their microbiomes who are responsible for mounting such powerful attacks against invasive microbes. The differential patterns of stability exhibited by P. astreoides across perturbed and non-perturbed field transplants suggest it is a 'glass cannon' whose microbiome is regulated by microbial processes, whereas A. cervicornis' consistent patterns of stability suggest that its microbiome is mainly regulated by host-level processes. Our results show that understanding how processes that operate at multiple levels of biological organisation interact to regulate microbiomes is critical for predicting the effects of environmental perturbations on host-microbial systems.