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Aoki Hawii 0085A 11063.Pdf Microbial Associations in the Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I AT MĀNOA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN TROPICAL PLANT PATHOLOGY May 2021 By Sayaka Aoki Dissertation committee: Mohammad Arif, Chairperson Brent Sipes Koon-hui Wang Fernando E. Vega Shefali Dobhal Ikkei Shikano Birendra Mishra, University Representative 1 © 2021, Sayaka Aoki ii Acknowledgements First and foremost, I am extremely grateful to my committee members; Dr. Mohammad Arif, Dr. Brent S. Sipes, Dr. Koon-hui Wang, Dr. Fernando E. Vega, Dr. Ikkei Shikano, Dr. Shefali Dobhal, and Dr. Birendra Mishra for their kind support and their thoughtful guidance during my Ph.D. in Tropical Plant Pathology. I would like to express a special acknowledgment to my advisor, Dr. Arif, who had accepted me as a transfer student and kindly supported me throughout my Ph.D. With his expertise and immense knowledge in bacteriology and bacterial taxonomy, I was able to achieve my goal of conducting research from the bacterial side of the story in the insect-symbiont system. Dr. Sipes and Dr. Wang had been highly supportive throughout my Ph.D. During this worldwide pandemic, I have faced difficulties in navigating my degree; however, with their support, I was able to complete my degree on time. I am extremely grateful for Dr. Vega, who has been kindly guiding me through my Ph.D. since 2016. My interest in symbionts and insect associations sparked when I came across one of his publications. I was ecstatic when he joined my committee panel. With his deep knowledge in coffee berry borer research, I was able improve my project to a level that I hoped for. I am also highly grateful to Dr. Dobhal, who has provided me with much guidance through my experiments. Especially with her vast knowledge in chemistry, I was able to navigate challenging experiments in the lab. I would also like to express my gratitude to Dr. Shikano and Dr. Mishra. I appreciate their inputs on my research, as well as providing me with many of their insights from various perspectives. I am immensely grateful for my supervisors and directors at the Hawaii agriculture research center, Dr. Chifumi Nagai, Dr. Ming-Li Wang, Stevie Warren, and Tyler Jones. I am extremely thankful for Hawaii agricultural research center for funding me through my Ph.D. and providing me with an opportunity to work as a research assistant in a coffee germplasm project. I am especially grateful for Dr. Nagai, who has been my mentor in science for many years. She provided me with support and guidance through my most difficult times. I also would like to express my gratitude to Dr. Wang. She had been understanding and supportive when I was having difficulty balancing work and experiments. iii I would like to thank all of the graduate students from the Tropical Plant Pathology program especially, lab members from Plant bacteriology; Gamze Boluk, Dario Arizala Quinto, Sujan Padel, Diksha Klair, Shu-Cheng Chuang, and Hanul Nathaniel Seo, for sharing their outstanding knowledge and skills in the whole genome sequencing, assembly, annotation, and another analytical part of my study. I am immensely grateful for their help, especially towards the end of chapter 4, my lab members provided me with much help to complete my experiments on time. I am very thankful for Dr. Mark Wright (Entomology) and Dr. Ania Wiecozrek (TPSS) for their support for my chapter 1, and Dr. Gordon M. Bennet (U.C Merced) for his guidance for the fluorescent in situ Hybridization assay and the analysis for chapter 2. I would like to express special gratitude for many other people who had helped me with experiments; Tina Weatherby and Dr. Marilyn Dunlap at the UH biological microscopy lab for assisting with confocal laser scanning microscopy assays, Dr. Anne Alvarez from Plant bacteriology lab for her kind guidance through my defense, and Andrea Kawabata, Jen Burt, and Marc Maisner at UH Kainaliu research station for sharing their insights on where to sample the coffee cherries on the Big Island. I am also grateful for all of the coffee growers who had kindly invited me to their farms to sample coffee berries. Representing all the coffee growers, I would like to give a special acknowledgment for Pepe Miranda, Tommy Greenwell (Kona), and John Ah Sun (Kau) I am grateful for my parents, Nobuhiko Aoki, M.D., Ph.D., and Sayoko Aoki for their support. My dear friend, Dr. Christine Lynch had stood by my side during the most challenging time of my life. With her support, I was able to achieve my goal. I also would like to give a special acknowledgment to my significant other, Robert Anthony Parr, who had been my rock throughout my Ph.D. He has provided me with moral, technical support, and many pieces of advice to navigate through my journey. This research was supported by NIH-COBRE, USDA, HARC, HDOA, and CTHAR. Sayaka Aoki 5/13/2021 iv Abstract Coffee (Coffea arabica and C. canephora; Rubiaceae) is one of the most important agricultural commodities in tropical and subtropical regions in the world, generating industries that surpass an estimated US$170 billion annually. The coffee berry borer (CBB), Hypothenemus hampei, is the most devastating insect pest of coffee worldwide. The insect was first reported in 1901, and it has invaded most coffee-producing countries, causing severe economic losses surpassing more than US$500 million annually. The coffee berry borer was first reported on Kona, island of Hawaii in 2010, and by 2020, it had been reported on Oahu, Maui, Kauai, and Lanai, causing significant economic loss in the coffee industry in Hawaii. Determining how the coffee berry borer became a coffee pest has been an area of interest due to the fact that it is the only insect to consume the coffee seeds inside the berry. Survival on the seeds therefore implies a mechanism to degrade caffeine. Insects have evolved a diversity of strategies to overcome challenges imposed by plants. One of the strategies to mitigate these challenges is to establish mutualistic associations with symbiotic microorganisms that could enable insects to thrive and reproduce within the unfavorable environments. These microbial symbionts associated with insects play pivotal roles in host survival, reproduction, host metabolism, and affect hosts’ biology and phenotypes via a multitude of functions, providing vital nutrients such as essential amino acids, nitrogen, vitamins, and sterols, breaking down cellulose and lignin materials that are hard to digest, influencing host plant usage, and mediating interactions with natural enemies. Recent studies have provided strong evidence of coffee berry borer-bacterial associations and the mechanisms, revealing the coffee berry borer has a range of associations with its bacterial symbionts for the survival and possibly affected its evolution and adaptations. Vega et al. (2002), revealed coffee berry borer associations with the maternally inherited bacterium Wolbachia from many countries. Ceja-Navarro et al. (2015) demonstrated that the coffee berry borer relies on caffeine-degrading bacterial symbionts in the alimentary canal in order to live in caffeine-rich conditions that are unfavorable for other insects. The caffeine-degrading microbiome reported by Ceja-Navarro et al. (2015) consisted of 13 bacterial species, and only one of these bacteria, i.e., Pseudomonas fulva, had the caffeine demethylase ndmA gene (methylxanthine N-demethylase A). When the insect was fed an artificial diet containing v antibiotics, they lost the ability to degrade caffeine, and their reproductive fitness was negatively affected (Ceja-Navarro et al. (2015). Additional investigations on the role of bacteria on the fitness of the coffee berry borer are needed in order to better understand the biology of the insect. The objectives of this study are to: (1) Determine the identity of bacterial species associated with the coffee berry borer in commercial coffee farms and wild coffee in Hawaii; (2) Explore the transmission mode of caffeine degrading bacteria by visualizing the bacteria within the insect eggs by fluorescent in situ hybridization (FISH) targeting the caffeine demethylation gene (ndmA); (3) Isolate and identify bacterial species associated with the eggs and determine if they are capable of breaking down caffeine; and (4) Conduct whole genome sequencing to identify them into species-level, and understand genome biology of bacterial species isolated from CBB eggs. vi TABLE OF CONTENTS ACKNOWLEDGEMENTS……………………………………………….……………………...iii ABSTRACT…………………………………………………………………………………….....v LIST OF TABLES……………………………………………………………………………..…ix LIST OF FIGURES………………………………………………………………………….…....x APPENDICES………………………………………………………………………………..…xiv CHAPTER 1. Bacterial taxa associated with the Coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae), in Hawai‘i Abstract………………………………………………………………………………...….1 Introduction…………………………………………………………………………..……2 Materials and Methods………………………………………………………………..…...7 Results………………………………………………………………………..……………9 Discussion………………………………………………………………….…………….13 Conclusion……………………………………………………………………………….15 Figures……………………………………………………………………………………17 Reference………………………………………………………………………..……….33 Appendix………………………………………………………………………...……….38 CHAPTER 2. Coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae), association with caffeine degrading
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