I UNIVERSITY of CENTRAL OKLAHOMA Edmond, Oklahoma
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UNIVERSITY OF CENTRAL OKLAHOMA Edmond, Oklahoma Jackson College of Graduate Studies Disease Surveillance and Projected Expansion in Climatic Suitability for Trypanosoma cruzi, the Etiological Agent of Chagas Disease, in Oklahoma A THESIS SUBMITTED TO THE GRADUATE FACULTY In partial fulfillment of the requirements For the degree of MASTER OF SCIENCE IN BIOLOGY By Matthew Dillon Nichols Edmond, Oklahoma 2018 i ACKNOWLEDGMENTS The completion of this project would not have been possible without the help and dedication from many people. I am thankful to my advisor, Dr. Wayne Lord, for his continual patience, guidance, encouragement, knowledge, and support. He fostered my interests in pathogenic microorganisms, notably parasites. This began when I enrolled in his parasitology course as an undergraduate and fell in love with the fascinating world of parasites. It was during this course that I decided to pursue a graduate degree and met with him to formulate a project that encompassed an emerging parasite in the United States. I would also like to thank the other members of my graduate committee, Dr. Michelle Haynie, Dr. Robert Brennan, and Dr. Vicki Jackson, for their constructive comments, project advice, and support throughout my thesis. I would like to thank Dr. Michelle Haynie for letting me use her laboratory to conduct my molecular work, laboratory training, and verifying my methods, for her positive reassurance during troubleshooting, and for patiently answering my questions and concerns. I would like to thank Dr. Chris Butler for his assistance with ecological niche modeling. I would like to thank Dr. William Caire for his guidance, mammalogy training, and assisting our team in safe field collection. I thank Dr. Creecy for his manuscript review and molecular analyses advice. I thank the Oklahoma Department of Wildlife Conservation and the landowners of the maternity roosts for giving us access for our field sampling. I thank UCO and Dr. Rebecca Williams for letting us stay at the Selman Living Laboratory during our field collection. I thank the numerous field research volunteers for their help in collecting samples and for decontamination: Wendy Monterroso, Sarah Vrla, Cristina Coffman, Chris Patton, Rikki Curto, Sarah Ranabeht, Brandon McDonald, Madison and Shari iii Schenfield, Josh Milky, and Stephanie and Erin Green. I thank Wendy Monterroso for being a reliable and fun researcher for the duration of this project and who brought great music for the long car drives to the Selman Living Laboratory. I thank my graduate friends at UCO for their support and creating a welcoming environment in the graduate lab. I thank my fiancé Madison Schenfield for her continual love and financial support through this project. I thank the UCO Department of Biology for employing me and providing financial assistance and a professional environment to conduct this research, as well as the Joe Jackson College of Graduate Studies. This research would not have been possible without financial support from the UCO College of Mathematics & Sciences; Student Transformative Learning Record (STLR); Research, Creative, and Scholarly Activities (RCSA) grants; the UCO Center for Wildlife Forensic Science and Conservation Studies (C-FACS); and the W. Roger Webb Forensic Science Institute at UCO. I would also like to thank the supportive faculty and my graduate friends at UCO for their encouragement and memories made during my degree. Lastly, I greatly thank my family for their endless love and support throughout my life. iv TABLE OF CONTENTS Acknowledgments………………………………………………………………………..iii List of Figures………...……………………………………………….……….....……..viii List of Tables………...……………………………………………….……….....…….….x List of Appendices………...……………………………………………….……….....….xi Thesis Abstract………...……………………………………………….……….....…….xii Glossary…..……………..…………………………………………………………...….xiv I. CHAPTER 1: THESIS INTRODUCTION…………………………….………………1 Literature Cited……………………………………………………………...…...45 Figure 1…..………………..……………………………………………………..79 Figure 2…..………………..……………………………………………………..80 Figure 3…..………………..……………………………………………….....81-82 Figure 4…..………………..…………………………………………………......83 Figure 5…..………………..……………………………………………………..84 Figure 6…..………………..……………………………………………………..85 II. CHAPTER 2: FIRST REPORT OF TRYPANOSOMA CRUZI IN A MEXICAN FREE- TAILED BAT (TADARIDA BRASILIENSIS) IN OKLAHOMA Abstract…………………………………………………………………………..86 Introduction…………..…………………………………………………………..86 Methods…..…………..…………………………………………………………..87 Results…..………………………………………………………………………..89 Discussion…..……………..……………………………………………………..90 v Acknowledgments…..…..………………………………………………………..90 Literature Cited…..……………..………………………………………………..92 Figure 1…..………………..………………………………………………….95-96 Figure 2…..………………..……………………………………………………..97 III. CHAPTER 3: PROJECTED EXPANSION IN CLIMATIC SUITABILITY FOR TRYPANOSOMA CRUZI, THE ETIOLOGICAL AGENT OF CHAGAS DISEASE, AND FIVE WIDESPREAD TRIATOMA SPECIES BY 2070 Abstract…………………………………………………………………………..98 Introduction…………..…………………………………………………………..99 Methods…..…………..…………………………………………………………102 Results…..………………………………………………………………………103 Discussion…..……………..……………………………………………………104 Acknowledgments…..…..………………………………………………………108 References…..……………..……………………………………………………109 Figure 1…..………………..……………………………………………………119 Figure 2…..………………..……………………………………………………120 Figure 3…..………………..……………………………………………………121 Figure 4…..………………..……………………………………………………122 Figure 5…..………………..……………………………………………………123 Figure 6…..………………..……………………………………………………124 Table 1…..………………..…………………………………………………….125 Table 2…..………………..…………………………………………………….126 vi IV. CHAPTER 4: GENERAL SUMMARY…..………..……………………………....127 Literature Cited…..……………..………………………………………………130 Appendices……………….……………..………………………………………………133 Appendix A1…..……………..…………………………………………………133 Appendix A2…..……………..…………………………………………………134 Appendix A3…..……………..…………………………………………………141 Literature Cited…..……………..………………………………………………157 vii LIST OF FIGURES CHAPTER 1 1. Trypanosoma cruzi life cycle illustrated with transmission and maturation in vertebrate (mammal) and invertebrate (triatomine) hosts. Obtained from Centers for Disease Control and Prevention 2015 https://www.cdc.gov/parasites/chagas/biology.html.............................................78 2. Schematic model summarizing the molecules involved in the parasite-host cell interaction process on the surface of a mammalian host cell and on a trypomastigote of Trypanosoma cruzi (obtained from Souza et al. 2010).……...79 3. A model of Trypanosoma cruzi intracellular invasion (obtained from Souza et al. 2010). The model represents three mechanisms of T. cruzi entry into a mammalian host cell. The first, the lysosome dependent pathway, which is initiated by targeted Ca2+ regulated exocytosis of lysosomes within the plasma membrane. The second mechanism is the actin dependent pathway in which the invading trypomastigotes penetrate the host cell via a plasma membrane expansion that promotes the assembly of a parasitophorous vacuole. Endosomes or lysosomes then fuse with the parasitophorous vacuole. The third mechanism involves a lysosome independent pathway, in which the trypomastigote enters a cell via plasma membrane invaginations that then accumulate PIP3 (a product of class I PI3K activation). The trypomastigote is contained in a vacuole formed from the plasma membrane and attracts early endosome markers (rab5 and EEA1). Lysosome markers are then attracted. The trypomastigote transforms into an amastigote when the parasitophorous vacuole lyses. The amastigote then divides within the cytoplasm (Souza et al. 2010).…………………………....80-81 4. Representation of various endocytic mechanisms involved when Trypanosoma cruzi invades a mammalian cell (obtained from Barrias et al. 2013). The formation and maturation of the parasitophorous vacuole relies on the fusion of lysosomes. The fusion of endosomes and lysosomes promotes the maturation of the parasitophorous vacuole through their acidification (Barrias et al. 2013).......82 5. The range of the migratory Mexican free-tailed bat (Tadarida brasiliensis; Wilkins 1989). This range spans multiple Trypanosoma cruzi endemic foci. During the fall, the population in Oklahoma migrates south through Texas and into Mexico along the Sierra Madre Oriental before returning in the spring to give birth at maternity roosts (Glass 1982)…………………………………...……….83 6. Study area map of northwest Oklahoma, USA illustrating Woodward, Major, and Woods counties in red. Mexican free-tailed bats (Tadarida brasiliensis) were sampled at maternity roosts within these three counties during the summer of viii 2017. The map was created using ArcMap (Environmental Systems Research Institute)…………………………….…………………...……………………….84 CHAPTER 2 1. The range of the migratory Mexican free-tailed bat (Tadarida brasiliensis; World Health Organization and International Union for Conservation of Nature and Natural Resources 2015 http://dx.doi.org/10.2305/IUCN.UK.2015- 4.RLTS.T21314A22121621.en). This range spans multiple Trypanosoma cruzi endemic foci. During the fall, the population in Oklahoma migrates south through Texas and into Mexico along the Sierra Madre Oriental before returning in the spring to give birth at maternity roosts (Glass 1982). The positive sample, sequence Woodward 1 matched closely to multiple Las Palomas Wildlife Management Area sequences on GenBank, which is along the migratory pathway. The representative T. cruzi lineages we used in the phylogenetic analysis are illustrated. Sampling occurred at three maternity roosts in Oklahoma during the summer of 2017………………………………………………….…………………...………95