Graduate Thesis Or Dissertation
 

Multiple Stressors Drive Changes in Coral Microbiome Diversity and Composition Demonstrating the Role of a Bacterial Symbiont in Microbial Community Sensitivity and Resilience

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  • On coral reefs, disturbances rarely occur in isolation. Global stressors such as increasing seawater temperature often coincide with local stressors like nutrient pollution. In the face of increasing anthropogenic stress, corals can function as environmental sentinels, although little is known about how multiple stressors interact to disrupt their associated bacterial communities and how symbiotic bacteria contribute to coral resistance and resilience to stress. Previous studies have shown that coral microbiomes under stress demonstrate shifts to more disease-associated states, increases in community variability, compromised function of beneficial microbiota, and selection for potentially pathogenic bacteria. Given that coral microbiota are thought to play an important role in host nutrient cycling and antimicrobial protection, it is important to understand how their response to individual and combined stressors can mitigate or exacerbate host susceptibility. My dissertation work coupled ecological experiments with DNA sequencing, bioinformatics, and multivariate statistics to describe compositional changes in coral microbiomes under various combinations of stressors and to infer the role of symbiotic bacteria in holobiont sensitivity and resilience to environmental disturbance. Ecological literature classifies interactions between combinations of individual stressors as synergistic, antagonistic, or having no interaction. We utilized common multivariate analyses to apply this multiple stressor framework to host-associated microbial communities. We conducted multiple stressor experiments both in mesocosm tanks and in the field on corals in Mo’orea, French Polynesia to evaluate how their microbiomes change compositionally with increasing and interacting levels of perturbation. We applied either no stress or single, double, or triple stressors of nutrient enrichment, simulated predation, and increased seawater temperature in mesocosm tanks to the coral Pocillopora meandrina for 21 days. We predicted that when sequentially adding stressors to the experimental system, we would observe a compounding increase in changes to the microbiome. In contrast, we found that microbiome disruption or variation from healthy controls does not scale positively with increasing number of stressors. In contrast to more heterogeneous communities that may be more robust to changes due to high diversity and functional redundancy, healthy P. meandrina controls were so dominated by Endozoicomonas, a proposed beneficial symbiont, such that any amount or type of stress was sufficient to increase community evenness. Single stressors of high temperature and scarring produced the largest shifts in community structure and additional stressors acted antagonistically to produce a less-than-additive response. We found that microbiome variability or dispersion increased with any number of stressors and community dysbiosis is characterized by a proliferation of opportunistic bacteria such as Rhodobacteraceae and Desulfovibrionaceae rather than a depletion of the dominant taxon, Endozoicomonas. To study this phenomenon in situ, we enriched corals on the reef before, during, and after a natural thermal stress event in 2016 to observe changes in the microbiome of Acropora, Pocillopora, and Porites corals undergoing concurrent temperature and nutrient stress. Concurrent work showed that corals exposed to nitrate exhibited more frequent bleaching, bleaching for longer duration, and were more likely to die. However, as observed in the tank experiment, we found that nutrients are less important for shaping the microbial community than temperature. The addition of nitrate and urea to the water column had no effect on the coral microbiome and did not interact with temperature. The three coral hosts displayed varying degrees of sensitivity to warm temperatures suggesting alternate strategies for coping with stress. Overall, post-stress microbiomes did not return to pre-stress community composition, but rather were less diverse and increasingly dominated by Endozoicomonas which could suggest its ability to utilize host metabolic products of thermal stress for a sustained competitive advantage against other microbial taxa. While we are only beginning to uncover the functional role of Endozoicomonas, these results suggest it may contribute to microbiome resilience to thermal stress. Endozoicomonas species associate with a wide variety of marine hosts, and within corals, are hypothesized to breakdown dimethylsulfoniopropionate (DMSP) which the coral host produces during thermal stress. To investigate this role and other potential roles in nutrition and defense, I used culture-independent methods of genome sequencing, metagenomics, to assemble the Endozoicomonas symbiont residing in Pocillopora meandrina corals in Mo’orea. Comparative genomics was subsequently conducted on all available Endozoicomonas genomes to better understand their shared and distinct functional characteristics. Despite their large genomes, Endozoicomonas species do not appear to contribute significantly to the cycling of carbon, nitrogen, or sulfur within the holobiont. Instead, they have many genomic features that could facilitate the maintenance of a stable symbiosis with their marine eukaryotic hosts. Only two Endozoicomonas species, not including our MAG (metagenome-assembled genome), encode genes involved in the breakdown of DMSP. Thus, we found no obvious genomic features that would suggest susceptibility or tolerance of this symbiont to thermal stress. In this dissertation, I demonstrate how a dominant member of the coral host-associated microbial community can drive patterns in community diversity and variability, ultimately influencing community resistance and resilience. While I investigate the genetic potential of this dominant taxon, genomic features that contribute to community sensitivity or resilience remain elusive. Overall, this work highlights the complexity of possible interaction outcomes for environmental stressors to coral reefs when assessed at the microbial scale and presents foundational patterns in microbiome dysbiosis and recovery that can inform reef persistence into the future.
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  • This dissertation work was funded by the NSF Graduate Research Fellowship and the Ford Foundation Dissertation Fellowship
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