Graduate Thesis Or Dissertation
 

Tracking Bacterial and Viral Shifts in Three Organisms to Shed Light on the Complex Role of Microbes in Coral Reef Health

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  • Stony corals are the ecosystem engineers of the vital, dynamic, and complex marine ecosystem known as coral reefs. Globally, coral reefs are undergoing degradation from multiple anthropogenic stressors. Coral reef organism holobionts, or the host along with its microbial components, are key to reef ecosystem success and functioning. Marine microbes can defend their hosts from pathogens, provide their hosts with advantageous functional capabilities, and contribute to nutrient cycling and availability in oligotrophic, or nutrient-poor, coral reefs. However, microbes may also contribute to or exacerbate coral disease adding to the stressors created under climate change. My dissertation focuses on how shifts in bacteria and viruses are linked to two reef stressors: bleaching and nutrient enrichment. Coral bleaching occurs when the photosynthetic coral-algal symbiont, Symbiodiniaceae, is expelled from the coral resulting in the loss of an important energy source for the coral. Research has shown that coral bleaching is tightly linked with increased ocean water temperatures, a phenomenon more common under anthropogenic climate change. An increased number of the global reefs are bleaching, and bleaching due to prolonged temperature stress can lead to coral death and degradation. Part of my research focuses on the role of viruses in coral bleaching and examines a bleaching paradox where a seemingly healthy non-bleached coral resides right next to a bleached coral. Using metagenomic sequencing and bioinformatic analysis we generated and analyzed viral sequences in both coral phenotypes. We found a significantly higher level of eukaryotic viruses in bleached corals compared to their non-bleached conspecific neighbors, and the non-bleached corals had higher levels of bacterial viruses, or phage, than eukaryotic viruses. This led us to hypothesize that eukaryotic viruses, infecting either the coral and/or its algal symbiont, may be taking advantage of or contributing to coral bleaching. We also assembled the first draft genome of a coral giant virus we believe is involved in coral bleaching. The second stressor that is highlighted in my dissertation is nutrient enrichment. Increased nutrients on coral reefs contribute to macroalgal growth that outcompetes corals for space and resources. This has led to the shift from coral- to algal-dominated reefs and contributes to the microbialization, or higher microbial abundance, of reefs, which can exacerbate coral disease. Much of my research focuses on the shifts in bacteria and viruses within three organisms that are part of an important reef trophic dynamic. These organisms include Stegastes nigricans damselfish, the turf algal matrix these fish farm, and the coral colonies the turf algae grows on. We conducted an experiment to expose these three organisms to a nutrient pulse in situ and used 16S rRNA amplicon sequencing to compare how their bacterial communities, or microbiomes, respond to a simulated anthropogenic nutrient enrichment. We found that coral microbiomes were the least diverse and the most susceptible to nutrient enrichment in that bacterial alpha and beta diversity significantly increased under nutrient enrichment. Fish and algal matrix microbiomes were not as strongly impacted by nutrient enrichment and instead saw changes in diversity over time. This showed that of the three organisms, coral microbiomes are predominantly affected by nutrient enrichment which has implications for overall coral health. We also found 51 of the same bacterial amplicon sequence variants in all three hosts indicating which microbes are shared or transmitted among reef organisms. However, methodologies to infer microbial diversity from environmental samples are challenging because 16S sampling diversity may not represent the total microbial diversity in the holobiont population and the uneven sequencing depth between samples requires normalization of the sequence data. Thus, to address how diversity inference and statistical hypothesis testing methodologies impact the biological interpretations of microbial data, we ran our coral, fish, and algal matrix 16S data sets through two statistical methodologies. One method uses a common but controversial method of rarefaction to normalize the data and an Analysis of Variance (ANOVA) to run hypothesis tests on how nutrient enrichment affects bacterial alpha diversity. The second method utilizes the packages Breakaway and DivNet which do not require rarefaction and include formulas to estimate unobserved taxa in diversity estimates and run hypothesis tests on alpha diversity. We found that each method had its advantages and disadvantages; rarefaction and ANOVA were quicker and more streamlined with other statistical tools like pairwise comparisons, while Breakaway and DivNet had longer computational times and could not compute estimates in the low diversity coral microbiomes. Therefore, we found that the more complex methodologies of Breakaway and DivNet attempt to represent population rather than sample diversity and do lead to differences in the statistical significance of our data, but such methods are not yet adequate for comparing microbiomes with varying levels of diversity. We further examined the microbial roles within coral reef organisms by sequencing the metagenomes of the fish and algal matrix samples from our nutrient enrichment experiment. In doing so we were able to identify and compare viral communities between samples from ambient and enriched conditions. We found interesting shifts within the eukaryotic viral group of nucleocytoplasmic large DNA viruses (NCLDV) and phage which strengthens that these viruses may have important roles under environmental changes. Namely, a significant increase in phage abundance and gene annotations occurred in nutrient enriched algal matrix samples indicating that phage take advantage of increased nutrients in complex open systems like the algal matrix. Phage shifts were not as prominent in fish samples, which represent a closed holobiont system, however shifts in NCLDVs indicated a decrease in the functional capacities of this viral group in fish. While more work needs to be done to confirm that these shifts are characteristic of both hosts under nutrient conditions, our research shows that viral shifts are common and detectable in coral reef organisms. Because host bacterial and viral communities are tightly linked with host health and ecosystem success, studying microbial shifts can give us valuable insights into their role in host and ecosystem health. My dissertation exhibits a breadth of research into both the viral and bacterial components of three reef organisms. We worked to expose which shifts may be indicators of varying host health conditions, like bleaching, or environmental stressors like nutrient enrichment. This dissertation aims to identify novel shifts in the microbial compositions of three integral reef organisms and add to the growing research on the role microbes play in ecosystem health.
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  • Ongoing Research
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  • 2021-12-14 to 2023-10-23

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