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Aetobatus Narinari) MICROBIOME VARIATION IN WILD VERSUS CAPTIVE EAGLE RAYS (AETOBATUS NARINARI) A Dissertation Presented to The Academic Faculty by Mary McWhirt In Partial Fulfillment of the Requirements for the Degree Master of Science in the School of Biological Sciences Georgia Institute of Technology August 2019 Copyright © Mary McWhirt 2019 MICROBIOME VARIATION IN WILD VERSUS CAPTIVE EAGLE RAYS (AETOBATUS NARINARI) Approved by: Dr. Frank Stewart, Advisor School of Biological Sciences Georgia Institute of Technology Dr. Lisa Hoopes Director of Research, Conservation and Nutrition Georgia Aquarium Dr. Brian Hammer School of Biological Sciences Georgia Institute of Technology Date Approved: July 18, 2019 ACKNOWLEDGEMENTS First, I would like to thank my advisor Dr. Frank Stewart for his guidance for allowing me the opportunity to learn a new set of skills. Your genuine enthusiasm for teaching and work creating academic programs such as CMDI and educational programs such as SWiMS are a constant reminder of the importance of education and community. I would also like to thank the members of the Stewart lab, in particular Zoe Pratte, for helping guide me along the way and their hands-on training during my time here at Georgia Tech. Thank you to the Georgia Aquarium and their commitment to conservation and research. Their partnership and support has allowed me to have a unique experience with in my work. Dr. Alistair Dove has been instrumental in the relationship between the Stewart lab and the Georgia Aquarium and I would not have had this opportunity without him. I would like to say a final thank you as well to the members of my thesis committee, Dr. Brian Hammer and Dr. Lisa Hoopes. In classes with Dr. Hammer, I gained a deeper understanding of microbial processes that has been beneficial throughout my program. Dr. Hoopes’ support from the Georgia Aquarium has been an integral part of this study, including sample collection and metadata. This work would not have been possible without your help. Thank you to everyone who made my time at Georgia Tech possible. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS iii LIST OF TABLES v LIST OF FIGURES vi LIST OF ABBREVIATIONS vii SUMMARY viii CHAPTER 1. Introduction 1 CHAPTER 2. Materials and Methods 5 2.1 Sample collection and lab processing 5 2.2 Illumina data processing 7 2.3 Statistical analysis 7 CHAPTER 3. Results 10 3.1 Niche-site microbiomes structure by environment 11 3.1.1 Taxa in gill microbiomes 14 3.1.2 Taxa in skin microbiomes 15 3.1.3 Taxa in cloaca microbiomes 16 3.2 Captive ray microbiomes throughout a year 17 3.2.1 Effect of a monogenean trematode infection on microbiomes 17 CHAPTER 4. Discussion 20 4.1 Conclusions 24 APPENDIX A. Metadata for ray and water samples 26 REFERENCES 29 iv LIST OF TABLES Table 1- Number of samples used in statistical analysis per type and 10 environment. Table 1- Permanova results of sample type and environment. 11 Table 3- Similarity percentages (SIMPER) beta diversity between 13 sample-habitat groups. Table 4A- Metadata for all ray and water samples. 26 v LIST OF FIGURES Figure 1- Non-metric MDS based on Bray-Curtis similarity of individually- 12 plotted duplicate spotted eagle ray samples. All samples are shown together and then separate gill, skin, and cloaca NMDS plots are grouped by habitat. Figure 2- Shannon Diversity Index and Chao1 as a representation of alpha 14 diversity between sample-habitat types. Figure 3. Non-metric MDS based on Bray-Curtis similarity of samples from 19 the Ocean Voyager exhibit. vi LIST OF SYMBOLS AND ABBREVIATIONS rRNA Ribosomal ribonucleic acid Na+ Sodium (+1) ion Cl – Chloride (-1) ion OTU Operational taxonomic unit NT Near threatened IUCN International Union for Conservation of Nature IACUC Institutional Animal Care and Use Committee µm Micrometer Cm Centimeter Kg Kilogram DNA Deoxyribonucleic acid PCR Polymerase chain reaction µl Microliter BSA Bovine Serum Albumin s Seconds bp Base pairs ASV Amplicon sequence variant QIIME Quantitative Insights Into Microbial Ecology SIMPROF Similarity profile routine NMDS Nonmetric multidimensional scaling vii SIMPER Similarity percentage OV Ocean Voyager viii SUMMARY The microbial communities (microbiomes) associated with elasmobranchs are currently not well-understood. The spotted eagle ray (Aetobatus narinari) is a slow-maturing ray that is globally distributed in tropical and warm-temperate waters, and is listed as near-threatened by the IUCN Red List. To evaluate how the environment shapes the spotted eagle ray microbiome, we used 16S rRNA Illumina sequencing to compare the microbiomes of the dorsal skin, gill, and cloaca from a ray population sampled in Sarasota Bay, FL to those from a captive population in the Ocean Voyager exhibit at Georgia Aquarium. Cloaca microbiomes of both populations had the lowest alpha diversity and highest beta diversity. The composition of the gill and skin microbiomes differed between captive and wild populations and are similar to, but distinct from, the water column communities while cloaca microbiomes are more divergent from that of the water. This pattern is consistent with that seen in teleost fishes and marine mammals. These results indicate a dual role for body niche and environmental conditions in shaping ray microbiomes and identify key taxa that may be important to the health of the rays. ix CHAPTER 1. INTRODUCTION Microbiomes of teleost fishes and marine mammals show a consistent pattern of having communities that are distinct within body-niche sites such as gills, skin, and gut. In teleost fishes these body site microbiomes, including those in contact with the external environment (e.g., skin, gills; 1), are influenced by host-specific factors including life- stage and diet, and gut microbiomes have been shown to become more complex after reef settlement (2). Marine mammals, including dolphins (order Cetacea) and sea lions (order Carnivora), also harbor microbiomes that vary by body site and host species (3). Knowledge of the impact of changes in environment or of captivity on host microbiomes could also lead to increased understanding of the functional role of niche-specific bacterial communities. A comparison of fecal samples from wild and captive Australian sea lions (Neophoca cinereal) found differences in bacterial communities between sampling sites, which could be attributed to colony dynamics, behavior, and foraging sites (4). In another marine mammal, the humpback whale (Megaptera novaeangliae) skin-associated microbiota appears to relate to geographic area and metabolic state, including a Psychrobacter that may be an influence of humpback whale seasonal migrations (5). With a migratory life-cycle, Atlantic salmon (Salmo salar) undergo an increase in phylogenetic diversity in the skin bacterial community during the transition from freshwater to seawater (6). These microbiome variations occurring during environment transitions suggest that microbiomes composition will differ between wild and captive marine animals. However, the extent to which environmental variation shapes composition might be expected to vary depending on the body site of the 1 microbiome, with more external sites (e.g., skin) affected to a greater extent by environmental drivers compared to internal sites (e.g., gut). To explore the relative roles of environment versus body site niche in shaping microbiome composition, this study compares the gill, skin, and cloaca microbiomes from a wild and captive population of a marine elasmobranch. As most studies of fish microbiomes have focused on teleost fishes, relatively little is known of microbiome structure and function in elasmobranchs, the subclass of Chondrichthyes (cartilaginous fish) that includes sharks, rays, and skates. This is a critical shortcoming given the wide distribution of elasmobranchs and their ecological relevance as top predators in marine food webs. In teleost fish, the microbiomes of diverse body sites have been shown to play roles in host defense against pathogens, chemical waste processing, and acquisition of essential nutrients from food (7, 8). The microbiomes of elasmobranchs, are hypothesized to play similarly important roles, which likely vary depending on body site. For example, the gills of elasmobranchs, as in teleosts, aid in ion (Na+ and Cl-) absorption, osmoregulation, acid-base regulation, and waste excretion (9, 10). It is possible that the unique physical and chemical conditions of the gills select for the presence of a specific community of microbes that aid in these functions. The mucus layer of the skin is also important to elasmobranch health. The detection of antibiotic activity in skin mucus from two ray species, the cownose ray (Rhinoptera bonasus) and the Atlantic stingray (Dasyatis sabina), suggests the possibility that the protective anti-pathogen role of skin mucus may be facilitated by resident microbes (11), potentially acting in concert with host-derived immune components such as lysozymes, lectins, and proteases (12). However, a full understanding of the functional 2 significance of elasmobranch microbiomes requires knowledge of factors shaping the microbiome composition. The processes shaping the microbiomes of elasmobranchs remain relatively uncharacterized, although some work has begun in this area. A study comparing the gut microbiomes of bony fish and 3 shark species found that the shark species shared core microbial operational taxonomic units (OTUs) but varied drastically in the number of observed OTUs (alpha diversity; 13). A study of shark and ray microbiomes
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