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Aurelia Aurita) and Evaluation of Their Tissues Using NMR-Based Metabolomics ABSTRACT DOERR, MARY. The Development of Euthanasia Techniques for Moon Jellyfish (Aurelia aurita) and Evaluation of their Tissues Using NMR-Based Metabolomics. (Under the direction of Dr. Michael K Stoskopf). Wild jellyfish are known to have significant impacts on coastal food web ecology and water quality. Advances in aquarium engineering and captive breeding capabilities have increased the availability of these delicate invertebrates for research purposes, although challenges persist in the management of water quality, nutrition, and disease. Moon jellyfish (Aurelia aurita) are an ideal species for novel investigations into jellyfish physiology due to their cosmopolitan nature, and their shared traits with most species of scyphozoan jellyfish. Metabolomics, the study of the small molecules involved in the pathways of cellular metabolism, is a rapidly growing area of study with applications in medicine, disease management, and marine systems biology. NMR spectroscopy allows for the evaluation of the full spectrum of metabolites from any tissue or biofluid and has the additional advantage of allowing for the determination of molecular structure from these samples, which can lead to the discovery of new biomolecules. Using NMR-based metabolomics to investigate jellyfish has the potential to generate new insight into their physiology and to add to the existing knowledge base in the field of marine metabolomics. This research project first investigates suitable methods of euthanasia for moon jellyfish destined for NMR spectroscopy, and then evaluates metabolic findings in captive specimens both healthy and diseased. The Development of Euthanasia Techniques for Moon Jellyfish (Aurelia aurita) and Evaluation of their Tissues Using NMR-Based Metabolomics. by Mary Doerr A thesis submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Master of Science Fisheries, Wildlife, & Conservation Biology Raleigh, North Carolina 2019 APPROVED BY: _______________________________ _______________________________ Michael K. Stoskopf Suzanne Kennedy-Stoskopf Committee Chair _______________________________ Tara M. Harrison DEDICATION For Mal, Boe, and Scarlett, my three biggest fans. ii BIOGRAPHY Mary Doerr is a graduate student and Master of Science candidate in Fisheries, Wildlife, and Conservation Biology at North Carolina State University. She works with Dr. Michael Stoskopf at the College of Veterinary Medicine doing metabolomics research in a variety of species, including vervet monkeys, hamadryas baboons, leatherback sea turtles, staghorn coral, and moon jellyfish. Her primary focus is moon jellyfish, for which she has developed sample processing protocols for NMR spectroscopy and collected metabolomics data. She lives in Raleigh, North Carolina with her three cats and will be joining the CVM class of 2023 in the fall to study zoo and wildlife medicine. iii ACKNOWLEDGMENTS I would like here to take a moment to express my deep gratitude to my advisor, Dr. Michael Stoskopf, for his unshakeable belief in my ability to complete this work even in its final hours, despite mounting evidence to the contrary. His guidance during my entire time here has helped me grow both as a student and as a scientist, and I consider myself very lucky to have had him as a mentor. I would also like to express my heartfelt appreciation for my committee members, Dr. Suzanne Kennedy-Stoskopf and Dr. Tara Harrison, who have provided me with unending support both academic and personal from the moment I stepped foot on campus all the way through to the completion of my degree. Their willingness to work with me through my struggles and their genuine celebration of my successes kept me out of the doldrums and helped bolster my sanity when I felt overwhelmed and out of place. I would also like to thank my colleagues and lab-mates, the Drs. Kate Archibald, Stasia Bembenek-Bailey, Meghan Louis, Jen Niemuth, and Lori Westmoreland, for their friendship, advice, commiseration, and practical know-how, which helped me both find and keep my footing as an odd duck in the Stoskopf lab. Many thanks are also due to Dr. David Morgan and Dr. Hanna Gracz for their contributions to the acquisition and interpretation of NMR data for all my various experiments, and for their patience in teaching complicated chemistry to a non-chemist. Finally, this work would not have been possible without the help and cooperation I received from the wonderful people at the North Carolina Aquariums, especially Dr. Emily Christiansen and Matt Babineau. Thank you. iv TABLE OF CONTENTS LIST OF TABLES ........................................................................................................................ vi LIST OF FIGURES ..................................................................................................................... vii Chapter 1: Review of Scyphozoan Biology and NMR-Based Metabolomics ......................... 1 Chapter 2: Evaluation of Euthanasia of Moon Jellyfish (Aurelia aurita) Using Simple Salt Solutions ................................................................................................................. 11 Abstract ............................................................................................................................ 12 Introduction ...................................................................................................................... 12 Materials and Methods ..................................................................................................... 12 Results and Discussion .................................................................................................... 13 Conclusion ....................................................................................................................... 14 Literature Cited ................................................................................................................ 15 Chapter 3: Metabolomic Evaluation of Abnormal Morphological Changes in Captive Moon Jellyfish (Aurelia aurita) Using NMR Spectroscopy ...................................... 16 Abstract ............................................................................................................................ 16 Introduction ...................................................................................................................... 16 Materials and Methods ..................................................................................................... 17 Animal Use and Euthanasia ....................................................................................... 17 Sample Processing ..................................................................................................... 18 NMR .......................................................................................................................... 18 Spectrum Analysis ..................................................................................................... 19 Results .............................................................................................................................. 19 Discussion ........................................................................................................................ 26 Control Jellyfish ......................................................................................................... 26 Cratered Jellyfish ....................................................................................................... 29 Folded Jellyfish .......................................................................................................... 29 References ................................................................................................................................... 30 v LIST OF TABLES Chapter 2 Table 1 Doses and euthanasia times for potassium chloride, magnesium chloride hexahydrate, and magnesium sulfate heptahydrate. ................................................. 13 Chapter 3 Table 1 Metabolites identified in the aqueous extracts of the stomach (S), bell (B), margin (M), and feeding arms (F) from unaffected and affected moon jellyfish (Aurelia aurita) grouped by metabolite class. ......................................................... 20 vi LIST OF FIGURES Chapter 3 Figure 1 Representative 1H-NMR spectra of aqueous extracts of bell (lowest, blue), margin (lower middle, red), stomach (upper middle, green) and feeding arms (top, purple) from unaffected moon jellyfish (Aurelia aurita). ....................... 22 Figure 2 Representative 1H-NMR spectra of aqueous extracts of bell (lowest, blue), margin (lower middle, red), stomach (upper middle, green) and feeding arms (top, purple) from cratered moon jellyfish (Aurelia aurita). ........................... 23 Figure 3 Representative 1H-NMR spectra of aqueous extracts of bell (lowest, blue), margin (lower middle, red), stomach (upper middle, green) and feeding arms (top, purple) from folded moon jellyfish (Aurelia aurita). .............................. 24 Figure 3 Representative stomach (S) spectrum from one cratered jellyfish showing chemical shifts from 0.0 to 4.6 ppm. The water peak is excluded to the left. Labeled peaks are as follows: Leucine (1), Valine (2), 2,2-Dimethylsuccinic acid (3), Lactate (4), Alanine (5), Citrulline (6), Thymidine (7), Proline (8), Glutamine (9), Dimethylamine (10), Malonate (11), Choline (12), Phosphorylcholine (13), Carnitine (14), Betaine (15),
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