Graduate Thesis Or Dissertation
 

Influence of the Environment and Morphology on Physiological and Genomic Homeostasis in a Temperate Cnidarian-microbe Symbiosis

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  • Climate change and other anthropogenic impacts are threatening the existence of millions of species around the globe. On western continental boundaries, the large-scale secondary process of upwelling, which brings low pH, deoxygenated, high nutrient seawater to the surface, is compounded by climate change, that together could drive some species to extinction. The ability to adapt and acclimate to change is key in determining which species will persist and which will perish. On the west coast of North America, the sea anemone Anthopleura elegantissima is a prominent member of the intertidal ecosystem. These anemones do not exist alone but are symbiotic with organisms across several phyla: eukaryotic microalgae, archaea, bacteria, fungi, and viruses. Together, a group of organisms living in symbiosis is called a holobiont. Taking a holistic point of view and studying the singular and synergistic biology in symbiotic systems are essential for understanding how these species will be affected by climate change. This dissertation examines aspects of each member of the A. elegantissima holobiont to gain a fuller understanding of the basic biology and impacts of climate change on this symbiosis. Symbiotic microalgae are an integral part of the coral-microalgal symbioses that build the foundation for productive and diverse reef ecosystems. The symbionts in these relationships are from a large family of dinoflagellates, the Symbiodiniaceae. Anthopleura elegantissima also joins in symbiosis with a symbiodiniacean, Breviolum muscatinei. Of particular interest, A. elegantissima can also be symbiotic with a green alga, Elliptochloris marina. In contrast to the well-studied Symbiodiniaceae, we know relatively little about E. marina. Currently, there is a species description and designation, stable state transcriptome, and a few physiological studies, but there remains a gap in the genomic resources for the species. In Chapter 2, I detailed my unsuccessful attempt to sequence and assemble the genome of E. marina with the goal to provide insight into the evolutionary underpinnings and maintenance of the symbiosis. In the future, a genome for this alga will be especially valuable as a comparator to dinoflagellate symbiont genomes. The microbiome of a holobiont is critical to consider when examining the ability of a host species to adapt and acclimate to a changing environment. In Chapter 3, the A. elegantissima gastrovascular cavity (GVC) microbiome was characterized to determine the effects of ocean acidification on the microbiome functional profile. Functional diversity within the GVC was much lower than the external seawater, suggesting that the GVC is a partially closed and highly regulated environment. With regard to ocean acidification (OA), there was no apparent influence on the microbiome function which could be related to the daily pH variations already experienced within the GVC caused by host respiration and symbiotic algae photosynthesis. Intracellular symbionts are removed from the environment. This separation requires the host species to engage nutrient and resource transport mechanisms to maintain an environment suitable for the symbionts. In Chapter 4, A. elegantissima carbonic anhydrases (CAs) were identified, and activity and gene expression measured to determine the effects of symbiotic state, anemone size, and light environment on CAs. These enzymes are responsible for maintaining internal pH homeostasis and, in organisms with photosynthetic symbionts, driving inorganic carbon concentration gradients to the site of photosynthesis. Regarding symbiotic state, A. elegantissima with E. marina had CA values similar to A. elegantissima without symbionts, suggesting that unaided diffusion and host respiration can keep pace with E. marina photosynthesis. Varying gene expression of different CA paralogs among symbiotic states supports the hypothesis that, in symbiosis, B. muscatinei and E. marina live in carbon-limited and relatively carbon-abundant environments, respectively. Host size and light level provided insight into the facultative nature of this symbiosis and the fact that most of the host’s nutrition is acquired through heterotrophic means. Overall, this work suggests that symbiotic A. elegantissima is largely heterotrophic in marked contrast to tropical symbiotic cnidarians. In summary, the work presented in this dissertation details specific aspects of each member of a temperate cnidarian-microbe symbiosis. From gene pathway to organism, the results of this dissertation underscore the necessity of a holistic view of symbiotic interactions and the value of looking at each part to make inferences about the whole.
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  • Ongoing Research
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  • 2021-02-12 to 2023-03-13

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