Graduate Thesis Or Dissertation
 

Impacts of Environmental Change on a Newly-characterized Symbiosis between a Novel Bacterial Parasite, Genus Aquarickettsia, and the Coral Acropora cervicornis

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https://ir.library.oregonstate.edu/concern/graduate_thesis_or_dissertations/x059cg217

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  • Coral reef ecosystems continue to be significantly altered by disease epizootics, but why some host populations remain resistant while others succumb to outbreaks remains unknown. Research across diverse animal and plant host systems has revealed that disease severity is strongly influenced by host genetics and by environmental influences on both host health and pathogen virulence. Further, microbiome imbalances (referred to as dysbiosis) characterized by the loss of commensal species and an increase in opportunists are often associated with negative host health consequences including increased disease susceptibility. These changes in microbiome ecological state may both be driven by and exacerbate stress from environmental change. Microbiome dysbiosis has repeatedly been found to occur in response to both global and local environmental stressors. The dual stressors of rising ocean temperatures and increased nutrient pollution have influenced both disease severity and prevalence by leading to increases in pathogen virulence and by reducing host immune capacity. Further, it has been suggested that environmental stress may trigger normally-commensal bacterial species to invade new host niches. These species may then outcompete beneficial microbial species, resulting in microbiome dysbiosis. This dissertation examines how two environmental extremes cause dramatic swings in the population of a dominant bacterial species in an essential reef-building coral. A bacterial species from the order Rickettsiales has been found to proliferate under nutrient‐enriched conditions to upwards of 80% of the microbiome of the coral genus Acropora. Though this bacterial species appears to require nutritional supplementation from its host, it does not appear to be pathogenic on its own, as it is tolerated at high abundances under normal environmental regimes. Nutrient enrichment, however, leads to increased abundance of this parasitic species, which is accompanied by reduced coral growth rates. Due to its dependency on nutrition from the host and its algal symbiont, this parasite is lost with thermal stress, causing total collapse of microbial community structure and allowing an influx of opportunistic bacterial species which subsequently lead to disease. We used both marker gene and concatenated gene phylogenetic trees to classify the phylogeny of the dominant parasite of A. cervicornis, and found that this species did not cluster closely with any named taxon in the order Rickettsiales. Sequences from this newly-identified species formed a distinct clade with other unclassified 16S rRNA sequences from diverse freshwater and marine hosts, with sufficient divergence to classify this clade as a new genus, which we named “Candidatus Aquarickettsia.” We assembled the genome sequence of “Ca. A. rohweri” from a sample of A. cervicornis, and found a reduced genome characteristic of an obligate symbiont. We posit, based on genome annotation, that A. rohweri requires host supplementation of most amino acids and possesses the capacity to import host ATP in exchange for ADP. This species also encodes numerous predicted two-component systems that are potentially involved in sensing extracellular conditions, and may play a role in the ability of A. rohweri to respond to environmental cues. To examine the distribution of this putative parasite across Acropora cervicornis genotypes currently used for restoration purposes, we classified microbiomes of 16 genotypes known to exhibit varying disease susceptibility. We found that disease-susceptible coral genotypes were characterized by a near-total dominance of A. rohweri, representing, on average, almost 90% of the detectable members of their microbial communities. In contrast, disease-resistant genotypes harbored A. rohweri populations comprising less than 5% of the microbiome, and exhibited significantly higher community evenness, with no single sequence variant exceeding 11% of the microbial community. We posit that the high abundance of parasitic A. rohweri infection in susceptible genotypes likely imposes a considerable burden on the host immune system, while the comparatively high microbiome diversity of other genotypes contributes to disease resistance by providing the host with a large arsenal of antimicrobial defenses. Further, we found that a thermal stress event homogenized microbiomes across all genotypes due to a significant decrease in populations of A. rohweri in susceptible genotypes. We hypothesized that this loss was related to the expulsion of the algal symbiont Symbiodiniaceae with thermal stress-induced bleaching, as A. rohweri may rely on Symbiodiniaceae for amino acid supplementation. Additionally, heat stress led to a sudden expansion of minor community members in disease-susceptible genotypes, with members of the order Alteromonadales and other potentially opportunistic genera significantly increasing in these samples, while these taxa did not increase significantly in disease-resistant genotypes. A nutrient enrichment experiment was conducted to assess the magnitude of change in abundance of Aquarickettsia in genotypes of Acropora cervicornis that under homeostatic conditions, naturally vary in abundances of Aquarickettsia. We determined that a disease-susceptible genotype of A. cervicornis (with high starting abundance of Aquarickettsia) exhibited significant declines in Simpson’s index of alpha diversity over the course of nutrient enrichment, and increases in the absolute abundance of Aquarickettsia (as assessed by qPCR) across all treatments. Differential abundance analysis, however, indicated that only treatments containing phosphate induced a shift in Aquarickettsia abundance relative to other taxa, suggesting that qPCR results may have been indicative of an increase in absolute abundance of all taxa. Corals of this genotype also exhibited suppressed growth rates in response to treatments containing phosphate. In contrast, a disease-resistant genotype of A. cervicornis (with low starting abundance of Aquarickettsia) were found to be dominated by an unclassified ASV belonging to Campylobacterales. Microbiomes of this coral genotype did not exhibit significant shifts in Simpson’s diversity in response to nutrient enrichment. While Aquarickettsia was found to respond to nutrient enrichment in these genotypes, relative abundances of this parasite remained very low (< 0.5%) at all timepoints. Although overall community structure did not change over the course of the experiment, individual taxa were found to respond to nutrient enrichment, including an increase in Ruegeria and Myxococcales, which have been identified as possible commensal or beneficial species, and a decrease in the dominant taxon from Campylobacterales. As microbial community composition and structure appeared to be stable in response to nutrient stress, but proportions of individual taxa shifted slightly, we hypothesize that these microbiomes represent an intermediate state between robust and flexible classes of coral microbiomes previously proposed in other studies. In this dissertation, I demonstrate that a dominant microbial community member of an essential reef-building coral species is highly responsive to changes in the environment. Shifts in the genus Aquarickettsia in response to thermal stress and nutrient enrichment lead to changes in community diversity and dispersion, which are associated with changes to host health and stress resilience. In contrast, coral genotypes with low abundance of this parasite exhibit more robust microbial community structure that is more resistant to dysbiosis. This body of work underscores the key role this bacterial taxon plays in the health of its host and presents new data to support a causative role of Aquarickettsia in acroporid disease susceptibility.
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  • Pending Publication
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  • 2021-09-21 to 2022-10-22

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