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Influence of Lab Adapted Natural Diet, Genotype, and Microbiota On INFLUENCE OF LAB ADAPTED NATURAL DIET, GENOTYPE, AND MICROBIOTA ON DROSOPHILA MELANOGASTER LARVAE by ANDREI BOMBIN LAURA K. REED, COMMITTEE CHAIR JULIE B. OLSON JOHN H. YODER STANISLAVA CHTARBANOVA-RUDLOFF CASEY D. MORROW A DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biological Sciences in the Graduate School of The University of Alabama TUSCALOOSA, ALABAMA 2020 Copyright Andrei Bombin 2020 ALL RIGHTS RESERED ABSTRACT Obesity is an increasing pandemic and is caused by multiple factors including genotype, psychological stress, and gut microbiota. Our project investigated the effects produced by microbiota community, acquired from the environment and horizontal transfer, on traits related to obesity. The study applied a novel approach of raising Drosophila melanogaster, from ten wild-derived genetic lines on naturally fermented peaches, preserving genuine microbial conditions. Larvae raised on the natural and standard lab diets were significantly different in every tested phenotype. Frozen peach food provided nutritional conditions similar to the natural ones and preserved key microbial taxa necessary for survival and development. On the peach diet, the presence of parental microbiota increased the weight and development rate. Larvae raised on each tested diet formed microbial communities distinct from each other. In addition, we evaluated the change in microbial communities and larvae phenotypes due to the high fat and high sugar diet modifications. We observed that presence of symbiotic microbiota often mitigated the effect that harmful dietary modifications produced on larvae and was crucial for Drosophila survival on high sugar peach diets. Although genotype of the host was the most influential factor shaping the microbiota community, several dominant microbial taxa were consistently associated with nutritional modifications across lab and peach diets. The effect that individual microbial taxa produced on the host varied significantly with changing environmental and genetic conditions. ii DEDICATION This dissertation is dedicated to my wife Shun Yan, who tirelessly supported me during the PhD journey and was my inspiration, during all these years. iii LIST OF ABBREVIATIONS AND SYMBOLS 16S rRNA 16S ribosomal ribonucleic acid gene CAFE Capillary feeder DGRP Drosophila Genetic Reference Panel DSPR Drosophila Synthetic Population Resource D Diet G Genotype NS Non-sterilized P Colorimetric assay plate PCR Polymerase chain reaction PHF Peach high fat diet PHFA Peach high fat autoclaved diet PHS Peach high sugar diet PHSA6 Peach high sugar autoclaved 6% diet PHSA11 Peach high sugar autoclaved 11% diet PR Peach regular diet R Regular diet RHF Regular high fat diet RHS Regular high sugar diet Ro Round iv RT Radioactive tracer S Sterilized T Treatment WGS Whole Genome Sequencing v ACKNOWLEDGMENTS I greatly appreciate the help of my academic advisor Laura K. Reed. Laura has not only guided me through academic and scientific work but has been very understanding and attentive mentor, with whom I could always share my sorrows and happiness. During the exhausting PhD journey, I avoided a need for professional psychological help largely due to Laura. I would like to express my appreciation to my committee members: John Yoder, who always served me as an example, with his research enthusiasm and tireless experimenting work, and who’s influence shaped my understanding of what does it mean to be a scientist; Julie Olson, who’s expertise in microbiology and microbial databases has navigated me through the microbiological part of my work, and who always encouraged me to think broader; Stanislava Chtarbanova-Rudloff, who has provided her guidance and research materials for dissections, to whom, I always have been able to come to talk about research and any other issue and who has been very sympathetic and encouraging, which meant a lot to me; Casey Morrow, who’s help with sequencing, troubleshooting, and obtaining funding has been crucial for generating our dataset, and who was always very supportive. I would like to thank Juan Lopez-Bautista, who provided his guidance for my whole academic career, from whom, I first learned what does it mean to do a research, and who was not only my teacher but also my friend. vi I would like to express my gratitude to my brother Sergei Bombin, who helped me with bioinformatical analysis, persevered all challenges of coming across the ocean with me, and a friendly competition with whom has kept me going through all these years. I would like to thank my students and researchers who put their time and effort in this work, without whom generating the sample size of more than 130,000 would be absolutely impossible, and who’s example fueled my ambitions: Owen Cunneely, Kira Ecikman, Abigail Ruesy, Rachael Cowan, Mengting Su, and Abigail Myers. As well as previous members of the team Caroline Hart, Ryan O'Rourke, and Kara MacIntyre. I appreciate the help of my colleagues: Logan Griffin, who significantly improved the sterilization method that I applied, and who became my friend; as well as Vishal Oza, Kelsey Lowman, Clare Scott, and YounJi Nam. I would like to thank the University of Alabama, College of Arts and Sciences, and the Department of Biological Sciences that provided me with financial resources without which, I would not be able to afford to finish this degree. I would like to thank my family; my mother Natalia Stroeva, without whom, I would not start my new life in the United States and most likely would not even become a scientist; my grandfather Vladilen Nichaev whose wisdom has guided me through my life, and from whom I learned most of my life skills; my grandmother Nadejda Nichaeva, and my sister Veronica Bombina for her cheerful example. I would like to thank my wife Shun Yan for her love and to whom this work is dedicated. vii CONTENTS ABSTRACT .................................................................................................................................... ii DEDICATION ............................................................................................................................... iii LIST OF ABBREVIATIONS AND SYMBOLS .......................................................................... iv ACKNOWLEDGMENTS ............................................................................................................. vi LIST OF TABLES .......................................................................................................................... x LIST OF FIGURES ..................................................................................................................... xiii CHAPTER ONE ............................................................................................................................. 1 INTRODUCTION ....................................................................................................................... 1 GOALS AND HYPOTHESES ................................................................................................. 13 CHAPTER TWO .......................................................................................................................... 16 INTRODUCTION ..................................................................................................................... 16 MATERIALS AND METHODS .............................................................................................. 19 RESULTS .................................................................................................................................. 28 DISCUSSION ........................................................................................................................... 55 CHAPTER THREE ...................................................................................................................... 66 INTRODUCTION ..................................................................................................................... 66 MATERIALS AND METHODS .............................................................................................. 71 viii RESULTS .................................................................................................................................. 79 DISCUSSION ......................................................................................................................... 148 CHAPTER FOUR ....................................................................................................................... 164 SYNTHESIS ........................................................................................................................... 164 CONCLUSIONS ..................................................................................................................... 178 FINAL NOTES ....................................................................................................................... 179 REFERENCES ........................................................................................................................... 180 ix LIST OF TABLES Table 2.1A: The difference in larvae phenotypes based on the diet ............................................. 30 Table 2.1B: The difference in fresh diets’ nutritional values ....................................................... 30 Table 2.1C: The difference in fresh diets’ nutritional values ....................................................... 30 Table 2.2: The influence of parental microbiota
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