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UC Riverside UC Riverside Electronic Theses and Dissertations UC Riverside UC Riverside Electronic Theses and Dissertations Title The Role of Detoxification Enzymes in Coral-Consuming Butterflyfish of Different Feeding Strategies From Hawaii and the Indo Pacific Permalink https://escholarship.org/uc/item/1sh3j6bd Author Maldonado, Aileen Publication Date 2015 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA RIVERSIDE The Role of Detoxification Enzymes in Coral-Consuming Butterflyfish of Different Feeding Strategies From Hawaii and the Indo Pacific A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Environmental Sciences by Aileen Maldonado August 2015 Dissertation Committee: Dr. Daniel Schlenk, Chairperson Dr. Jay Gan Dr. Michael Anderson Copyright by Aileen Maldonado 2015 The Dissertation of Aileen Maldonado is approved: _____________________________________________________________ _____________________________________________________________ _____________________________________________________________ Committee Chairperson University of California, Riverside Acknowledgments There are many people that made this work possible and were invaluable in this project. First, I would like to thank my advisor Dr. Daniel Schlenk for guiding me to work on butterflyfish and detoxification as described in this thesis. I would also like to thank him for providing supervision, financial support, networking opportunities, and collaborations over the past four years. My committee members, Dr. Michael Anderson and Dr. Jay Gan, were also incredibly supportive throughout my project. Additionally, this work would not have been possible without the help of many collaborators. I would like to thank Dr. Gary Ostrander for his laboratory space and financial support for this project, Dr. Marc Slattery, Dr. Deborah Gochfeld, and Dr. John Rimoldi at University of Mississippi for providing compounds and edits without which this project would not have been possible, and Dr. Jon-Paul Bingham, Dr. Luc Rugee, and Dr. Robert Richmond for your lab space and immense support. I would also like to thank Dr. Ehun Hoh for allowing me to use your LCMS/MS and for Kayo Watanabe for helping me run the samples. I would also like to thank Dr. Morgan Pratchett and Jessica Nowicki for collecting fish in Australia. We thank Dr. Andrew Rossiter and the staff of the Waikiki Aquarium for providing laboratory facilities and technical expertise. I would also like to thank Dr. Malin Celander (University of Gothenburg) and Dr. Donald R. Buhler (Oregon State University) for providing the anti-CYP antibodies. Many former and present members of the Schlenk laboratory also aided in the completion of this work. In particular I would like to acknowledge Dr. Ramon Lavado for his technical support, extensive knowledge, and HPLC fixing expertise. My lab mates iv and friends, Navneet Schworetzky, Dr. Lindley Maryoung, Anita Küpper, Graciel Diamante, and Allison Kupsco, Dr. Alicia Taylor, Dr. Lauren Hale, and Lindsey Sauma were wonderful in helping to solve problems, as well as provided support and entertainment to help keep me motivated. I would like to thank the undergraduates Bronte Crook, Jenna Harlacher, Danielle Garcia, Micheala Nuestro and Chelsea Wolke that helped me throughout the project caring for fish and running assays. The fish collectors also made this project possible Matt, Denis, DJ, Jeff, and Jeremy. I would like to thank my dad Alberto Maldonado, Mom Mariella Maldonado, and sister Kianna Maldonado for their support throughout my years of education financially, emotionally, and mentally. Without my families love and support and I would not have been able to accomplish this project. I would especially like to Stephen Fallon for spending countless hours listening to me, supporting me, grammar editing my papers, and loving me throughout this project. Stephen Fallon you have been there day in day out and I could not have done this without you, thank you so much. v Dedication This dissertation is dedicated to my family, my friends, and my boyfriend Stephen Fallon. All these people have read through long papers, given me advice, and encouraged me throughout my degree, I am eternally grateful. vi ABSTRACT OF THE DISSERTATION The Role of Detoxification Enzymes in Coral-Consuming Butterflyfish of Different Feeding Strategies From Hawaii and the Indo Pacific by Aileen Maldonado Doctor of Philosophy, Graduate Program in Environmental Sciences University of California, Riverside, August 2015 Dr. Daniel Schlenk, Chairperson A primary mechanism reef predators use to cope with dietary toxins is through detoxification. Detoxification enzymes cytochrome P450 (CYP) (specifically CYP3 and CYP2) were found in higher concentration in butterflyfish that preferentially feed on allelochemically rich corals. Butterflyfish (Chaetodon sp.) have unique feeding strategies with some species being generalist feeders and others feeding on several species of chemically-defended coral. This research elucidates the coevolutionary relationship between butterflyfish and corals by understanding the role detoxification enzymes play in allowing butterflyfish of differing feeding strategies to consume toxic allelochemicals produced by corals. To examine this issue detoxification enzymes CYP1, 2, 3, epoxide hydrolase, glutathione S-transferase (GST) and UDP-glucuronosyltransferase (UGT) were analyzed in butterflyfish of species C. kleinii, C. lunulatus C. auriga and C. vii unimaculatus from Hawaii and Australia. These results have indicated that species consuming soft coral have significantly increased CYP2 and 3A expression and catalytic activity, and GST activity. Also hard coral feeding preference on Porites spp. over Acorapora spp. had significant CYP2 and 3A expression and catalytic activity, and GST activity. Further investigation into hard coral Porites lobata and the feeding deterrent compound homarine (found in the coral extract), found that oral exposure to P. lobata homogenate significantly induced content and catalytic activity of CYP2 and CYP3A, by 2-3 fold and by 3-9 fold, respectively, in preferred specialist C. multicinctus, but not in C. auriga or C. kleinii. Homarine caused a significant decrease of CYP3A and CYP2 at the high dose in C. kleinii and 60-80% mortality in that species. Soft coral Sinularia maxima and isolated compound 5-Episinuleptolide (5ESL) were deterrent to butterflyfish generalist feeders, but not specialists. Oral exposure to 5-ESL caused 100% mortality on the hard coral specialist C. multicinctus and the least toxicity on soft coral specialist C. unimaculatus, correlated with the incredible induction of CYP3A catalytic activities and concentrations, NADPH dependent metabolism, and CYP3A identified metabolite. My results indicate that dietary exposure to coral homogenates and the feeding deterrent constituent within these homogenates caused species-specific modulation of detoxification enzymes consistent with the prey selection strategies of generalist and specialist butterflyfishes. viii Table of Contents Chapter 1: Introduction...............................................................................1 Chemical Arms Race..........................................................................3 Biotransformation...............................................................................4 Cytochrome P450 monooxygenase....................................................6 Other Detoxification Enzymes...........................................................12 Butterflyfish........................................................................................16 Impacts of Feeding Strategies on Detoxification and Fitness............21 Corals and Chemical Defensive Allelochemicals..............................23 Secondary Metabolites and Chemical Defense..................................26 Overview............................................................................................30 References..........................................................................................32 Chapter 2: The Role of Biotransformation Enzymes in Diet of Coral-consuming Fish in Hawaii versus Australia. Abstract..............................................................................................45 Introduction........................................................................................46 Materials and Methods.......................................................................50 Results................................................................................................58 Discussion..........................................................................................66 References..........................................................................................77 ix Chapter 3: The Role of Cytochrome P450 in Biotransformation of a Hard Coral (Porites Lobata) Extract and Homarine in Butterflyfishes Abstract..............................................................................................84 Introduction........................................................................................85 Materials and Methods.......................................................................87 Results................................................................................................93 Discussion..........................................................................................98 References..........................................................................................105
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