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Exploring the Ecology of Complex Microbial Communities Through EXPLORING THE ECOLOGY OF COMPLEX MICROBIAL COMMUNITIES THROUGH THE COCKROACH GUT MICROBIOME by KARA ANN TINKER (Under the Direction of Elizabeth A. Ottesen) ABSTRACT Microbes represent the majority of biomass and diversity found on planet earth and are essential to the maintenance of global biochemical processes. However, there is still much that is unknown about what drives the formation and maintenance of complex microbial communities. Here, we explore the ecology of complex microbial communities through an examination of the cockroach gut microbiome. The cockroach gut microbiota is highly complex and is analogous to the human gut microbiome in structure, function, and overall diversity. Insects in the superorder Dictyoptera include: carnivorous praying mantids, omnivorous cockroaches, and herbivorous termites. We use 16S rRNA amplicon sequencing to survey the structure and diversity across of gut microbiota 237 cockroaches in the Blattodea order. Results show that host species plays a key role in the gut microbiota of cockroaches. This suggests that cockroach host-microbe coevolution preceded the emergence and possibly facilitated the dietary specialization of termites. Previous work suggests that diet is plays an important role in shaping the Blattodea gut microbiome. We conducted a series of dietary perturbations to determine the effect of diet on the structure of the cockroach gut microbiome. We found the cockroach hosts a taxonomically stable gut microbiome, which may aid the host in survival during low-food and/or starvation events. This stability is highly unusual and has not been found in any other animal that hosts a complex gut microbial community. This suggests that cockroaches have evolved unique mechanisms for establishing and maintaining a diverse and stable core microbiome. Cockroaches and termites are known for their diverse gut microbiota, however little is known about the praying mantid gut microbiome. In order to better understand the mantid gut microbiome, we conducted a 16S rRNA gene-based study of gut microbiome composition in adults and late-instar larvae of three praying mantis species. We found that few microbial lineages are shared among praying mantids and cockroach relatives. This adds further support for the role of microbes in facilitating dietary specialization among insects in the superorder Dictyoptera and is an important area for future study. INDEX WORDS: Dictyoptera, Blattodea, cockroach, insect, invertebrate, microbial ecology, environment-host-microbe, host-microbe, gut microbiome, microbiome, 16S rRNA sequencing, metatranscriptomics EXPLORING THE ECOLOGY OF COMPLEX MICROBIAL COMMUNITIES THROUGH THE COCKROACH GUT MICROBIOME by KARA ANN TINKER BS, North Carolina State University, 2012 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2018 © 2018 Kara Ann Tinker All Rights Reserved EXPLORING THE ECOLOGY OF COMPLEX MICROBIAL COMMUNITIES THROUGH THE COCKROACH GUT MICROBIOME by KARA ANN TINKER Major Professor: Elizabeth A. Ottesen Committee: Robert Maier Mary Ann Moran Joy Doran-Peterson William Whitman Electronic Version Approved: Suzanne Barbour Dean of the Graduate School The University of Georgia May 2018 DEDICATION To my grandfather, for all of the conversations about life and science that we were never able to have. To my father, for his willingness to listen. To my mother, for her unwavering confidence in my integrity and ability. And to my brothers, for their humor and love. iv ACKNOWLEDGEMENTS I would like to thank my advisor, Liz Ottesen, for the leap of faith she took when agreeing to let me rotate in her new lab before we had even met in person. I am so grateful for your patience and support throughout the years. I would also like to my committee members Mary Ann Moran, Barny Whitman, Joy Doran- Peterson, and Rob Maier for their scientific guidance and confidence in me. I would also like to thank the microbiology department faculty and staff for their support and assistance, with special thanks to Anna Karls, Jonathan Frye, Sophia Flemming, and Dale Boyer. There are many people who supported and encouraged me along the way. I treasure each person who helped me celebrate successes, mourn failures, and who were there for every moment in between. I would like to especially thank my family, friends, cohort, lab mates, and 5th floor lunch buddies. I would like to especially acknowledge the support of Jack and Gwena Tinker, Jenae Cleghorn, Caitlin Reeves Williams, Kelsey Hodge-Hanson, Amber Enriquez, Trace Borchardt, and Morgan Teachey. Finally, I would like to thank Maia Call. I am lucky that I have a friend who knows my life so well. Without your love and support, I would have stopped growing a long time ago. ♥ v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .............................................................................................................v CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .....................................................1 1.1 Acquisition of gut microbiota ............................................................................2 1.2 Host-microbe interactions ..................................................................................3 1.3 Influences on the gut microbiome ......................................................................5 1.4 Zooming Out: Cockroaches in the Ecosystem ...................................................7 1.5 Addressing the gaps: Objectives ........................................................................7 1.6 References ..........................................................................................................9 2 HOST PHYLOGENY PLAYS A KEY ROLE IN SHAPING THE COCKROACH GUT MICROBIOME ..................................................................................................18 2.1 Abstract ............................................................................................................19 2.2 Introduction ......................................................................................................19 2.3 Methods............................................................................................................20 2.4 Results ..............................................................................................................24 2.5 Dicussion .........................................................................................................28 2.6 Acknowledgements ..........................................................................................29 2.7 References ........................................................................................................30 2.8 Tables ...............................................................................................................36 vi 2.9 Figures..............................................................................................................37 3 THE CORE GUT MICROBIOME OF THE AMERICAN COCKROACH, PERIPLANETA AMERICANA, IS STABLE AND RESILIENT TO DIETARY SHIFTS ........................................................................................................................45 3.1 Abstract ............................................................................................................46 3.2 Importance .......................................................................................................46 3.3 Introduction ......................................................................................................47 3.3 Introduction # 3.4 Methods............................................................................................................48 3.5 Results ..............................................................................................................53 3.6 Discussion .......................................................................................................59 3.7 Acknowledgements ..........................................................................................62 3.8 References ........................................................................................................63 3.9 Tables ...............................................................................................................69 3.10 Figures............................................................................................................70 4 THE PRAYING MANTIS HOSTS A HIGHLY VARIABLE GUT MICROBIOME DOMINATED BY MANTID-SPECIFIC BACTERIAL LINEAGES ......................74 4.1 Abstract ............................................................................................................75 4.2 Introduction ......................................................................................................75 4.3 Methods............................................................................................................77 4.4 Results ..............................................................................................................80 4.5 Discussion .......................................................................................................82 4.6 Acknowledgements ..........................................................................................84 4.7 References ........................................................................................................85 vii 4.8 Tables ...............................................................................................................92
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