Investigating the drivers of microbial community dynamics in Caribbean reef-building corals

Abstract

Coral-associated microbial communities (microbiomes) have been increasingly recognized as important contributors to key functions that promote the health and persistence of their hosts. Rapid global climate change can impact the coral microbiome symbiosis and lead to negative shifts in microbial community structure that can ultimately lead to coral disease and the destruction of the coral reef. Conversely, microbes may contribute positively to coral resistance and resilience by rapidly adapting to varying environmental conditions. This dissertation uses a combination of survey, experimental, and theoretical methods to (i) define the characteristics of a healthy coral microbiome, (ii) identify the underlying mechanisms generating variability in coral microbiomes, and (iii) evaluate how processes operating at multiple levels of biological organization interact to regulate the microbiome in response to external perturbations and disease incidence. Chapter 2 describes a field survey in which I examined the natural microbiome variability associated with six Caribbean coral species (Acropora cervicornis, A. palmata, Diploria labyrinthinformis, [Pseudodiploria] D. strigosa, Porites astreoides, and P. furcata) from three genera at multiple reef sites over a period of one year. I identified differences in microbiome composition between coral genera and species that persisted across geographic and temporal scales, indicating that local processes such as coral host identity likely plays a strong role in microbiome structure. In addition, utilizing network analysis, I demonstrated that the strength of host identity over microbiome composition varied across coral genera. I further identified ubiquitous bacterial phylotypes (i.e., core microbiome) for each coral genus, and revealed that bacterial communities in corals show taxonomical, and potentially functional, redundancy in both the whole community and the core coral microbiome. Chapter 3 builds on this finding by assessing whether natural variability across coral genera is indicative of resistance to external disturbances. Using a common-garden field experiment, I identified and quantified the microbial community response after exposing three coral genera (A. cervicornis, D. strigosa, and P. astreoides) to a pulse perturbation consisting of a large dose of broad-spectrum antibiotics. I showed that all coral host microbiomes exhibited a high degree of resistance to the disturbance, however, the stability of their microbial communities varied across coral host species. Coral species that previously displayed the highest variability and community turnover (Chapter 2), here, exhibited the greatest resistance to the experimental perturbations. To resolve this apparent paradox, I developed a novel stage- structured mathematical model of host-microbial dynamics that showed post-disturbance stability depended on whether microbiome control (via antimicrobial compounds) was regulated by the coral host or within the microbiome itself. These results highlight that understanding how processes operate across multiple levels of biological organization interact to regulate microbiomes is critical to both predict and mitigate the effects of environmental variation. Finally, host-microbiome interactions play an important role in a host's susceptibility to disease, therefore, predicting when and how healthy microbiome symbioses break down represents an essential challenge for coral disease ecology. To address this issue, Chapter 4 utilized a tank-based transmission experiment using White Band Disease (WBD) on the staghorn coral A. cervicornis. This chapter compares the effects of broad-spectrum antibiotics and two rounds of exposure from healthy and diseased coral tissue homogenates on microbiome diversity and structure over time. This exposure treatment allowed me to test key factors associated with deterministic and stochastic microbial community assembly. I identified a positive legacy effect of antibiotics on coral-microbiome diversity and health that persisted through time. I determined there was a weak probiotic effect, and that a more specific and targeted exposure to beneficial microbes is necessary to potentially establish a positive probiotic effect. I further determined there was no evidence of a priority effect, as microbes from healthy hosts were unable to suppress the invasion of microbes from diseased hosts purely by colonizing first. Thus, the outcome of competition does not depend on initial conditions and is therefore more predictable.--Author's abstract