Date of Award
2024
Degree Type
Dissertation
Degree Name
Doctor of Philosophy in Oceanography
Department
Oceanography
First Advisor
Roxanne A. Beinart
Abstract
Mutualisms are a cornerstone of ecological and evolutionary processes, profoundly influencing ecosystem diversity and functionality. At deep-sea hydrothermal vents, mutualistic microbial symbionts inhabit a variety of host structures, including the gill tissues of bivalves, the trophosomes of tubeworms, esophageal glands in certain vent snails, and epibiotic layers on crustaceans, and facilitate the primary production of organic matter through chemosynthesis. This process forms the base of the hydrothermal food web, supporting a dense community of animals in an otherwise oligotrophic deep ocean. However, the population structuring of these symbionts is essential to understanding their resilience, adaptability, and role in ecosystem stability. Population structure reveals how symbiont strains respond to environmental changes, whether through genetic adaptation, shifts in distribution, or associations with different hosts, which directly impacts the stability of mutualisms at the base of these ecosystems. For instance, symbionts with greater genetic diversity or robust dispersal potential may support hosts more effectively under stress, while structured populations may be more vulnerable to disruptions such as deep-sea mining, potentially destabilizing the entire ecosystem. Given that many vent animals are listed as endangered or vulnerable on the IUCN Red List, understanding these dynamics is critical for predicting how symbionts and their hosts might respond to environmental and anthropogenic pressures. This dissertation employs molecular and bioinformatic techniques to explore how symbiont lifestyle, biogeography, phage inter-actions, and environmental disturbances shape symbiont availability, acquisition processes, population genomics, and host-symbiont dynamics in deep-sea hydrothermal vent ecosystems.
Hydrothermal vent symbioses are predominantly established through horizontal acquisition of microbial symbionts from the environment. However, very little is known about free-living symbionts, whether they are genetically or functionally distinct from their host-associated counterparts, and whether any genomic differences (or the lack thereof) can elucidate acquisition processes. Therefore, to address this knowledge gap, in Chapter 2 we assembled the first genomes of gammaproteobacterial symbionts from Alviniconcha hessleri from the Mariana Back-Arc Basin vent fields. By applying phylogenomic and population genomic methods like single nucleotide polymorphism (SNP) calling, we assessed sequence and gene content variation between free-living and host-associated symbionts. Our results suggested that symbiont acquisition and release may occur sporadically throughout the host’s lifetime, and that symbiont population structure was primarily driven by biogeography, even on small scales (~5m), as opposed to lifestyle. This indicates that geographic isolation and/or adaptation to local habitat conditions were important determinants of symbiont population structure. Moreover, our results show that the observed biogeographic strain-level gene-content variation in the symbionts was driven largely by bacteriophage interactions.
Consequently, Chapter 3 examined the role of contemporary and historic bacteriophage infections in shaping the population structure and host-symbiont dynamics across five different animals and their gill-associated endosymbionts across six Lau Ba-sin hydrothermal vent fields. We investigated whether phage infections varied within and among species and considered whether these phage infections may represent advantageous or disadvantageous associations. Our results indicated that historic infections, as revealed by CRISPR spacer content, contributed to some of the observed strain-level variation. Furthermore, all but one symbiont species in this study lacked prophage infections entirely. This was an unexpected result, as prophage-harboring bacteria are common at hydrothermal vents
To better understand how phage interactions vary through time, and to better elucidate whether these prophage infections might represent beneficial or harmful infections, in Chapter 4 we conducted a temporal analysis of symbiont-phage interactions at the Lau Basin from 2009, 2016, and 2022. As observed in Chapter 3, only one symbiont species harbored prophages. Two temperate phage species persisted over time, suggesting that they might indeed confer benefits to the bacteria, possibly through providing super immunity, opportunities for horizontal gene transfer, and/or population control, despite lacking traditional genetic signatures like auxiliary metabolic genes (AMGs), though no direct evidence for these alternative benefits was identified. Furthermore, in 2022 there were several new strain-specific prophage species, which corresponds with the observed strain-specific CRISPR spacer content in our symbiont genomes.
In Chapter 5, we aimed to improve our understanding of the abundance and distribution of free-living symbionts within and between vent fields at the Lau Basin. In December 2019, the Hunga Tonga-Hunga Ha’apai submarine volcano explosively erupted, resulting in a blanket of ash upon some of the Lau Basin hydrothermal vent fields, decimating the animal communities. We, therefore, expanded our study to investigate whether the eruption affected the availability and distribution of environmental symbionts. We collected free-living symbiont samples using a Suspended Particulate Rosette (SuPR) Sampler and used a spike-in technique with our DNA extractions to obtain absolute abundance for our 16S rRNA analyses. We found that some symbiont species were entirely absent from the water column, though unlikely a consequence of the eruption. Interestingly, we observed elevated symbiont abundances at an active vent field where animal populations had been completely decimated, suggesting a potential mass release of symbionts following host mortality. Additionally, high symbiont abundances were detected hundreds of meters away from known active venting or animal communities, indicating widespread dispersal and an ability to persist in absence of chemical reductants.
Recommended Citation
Hauer, Michelle A., "INVESTIGATIONS INTO THE POPULATION STRUCTURE, DISTRIBUTION, AND PROPHAGE-LINKED PROCESSES IN DEEP-SEA HYDROTHERMAL VENT SYMBIONTS" (2024). Open Access Dissertations. Paper 1717.
https://digitalcommons.uri.edu/oa_diss/1717
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