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Host-Microbial Symbiosis Within the Digestive Tract of Periplaneta americana. Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Benjamin C. Jahnes Graduate Program in Microbiology The Ohio State University 2020 Dissertation Committee Professor Zakee Sabree, Advisor Professor Kelly Wrighton Professor Virginia Rich Professor Rachelle Adams 1 Copyrighted by Benjamin C. Jahnes 2020 2 Abstract Cockroaches as a model system allow us to explore a self-contained microbial community of incredible complexity, with the gut alone housing numerous members of the Eukarya, Bacteria, and Archaea, often in close symbiotic association with one another. This diversity provides us with the opportunity to examine a plethora of microbe/microbe and microbe/host interactions, with recent work in this area reviewed here. The ease of rearing the cockroach and its great resilience allows us to look at the cockroach as a blank slate, in the absence of gut microbiota, and set a baseline for growth through the establishment of germ-free insects. Assembling an aseptic isolation habitat of low cost and complexity is shown to aid in the maintenance of germ-free insects and allows for the selective reintroduction of gut bacterial isolates to the cockroach. The germ-free cockroach provides the potential to systematically examine interactions between the cockroach and the diversity of life that can be isolated from within the gut of the insect. In this work the germ-free cockroach is inoculated with gut microbiota through coprophagy and compared to wild-type cockroaches to examine the degree to which this behavior serves to provision the gut with symbiotic taxa, and examine the extent of bacterial stimulation of growth and development in wild-type compared to germ-free insects. A brief inoculation by coprophagy appears to endow cockroaches with a subset of the wild-type microbial community that is sufficient to induce growth phenotypes of ii the hindgut that are significantly different from, but intermediate to germ-free and wild- type cockroaches. Histological sectioning along the gut further refines the site of microbial stimulation of host gut development to the posterior midgut and anterior hindgut. Finally, several closely related and strongly host-associated cockroach gut Bacteroides are examined in relation to common mammalian gut Bacteroides, to examine to what extent insect Bacteroides have retained traits that may be required for host association and gut colonization. These native Bacteroides are then introduced to germ- free cockroaches in a defined community to examine genus-specific dynamics of gut colonization and host-growth promotion. The four reintroduced Bacteroides prove to have variable abilities to colonize a naïve gut environment and don’t positively contribute to cockroach development, in a monogeneric community. This demonstrates that more complex microbial community level interactions among gut microbiota and successional dynamics may contribute to preparing the gut environment for colonization by native gut microbiota, and host adaptation alone doesn’t guarantee microbe/host mutualism. iii Dedication I dedicate this work to my mom and dad who fostered a sense of wonder and encouraged my curiosity in the natural world and my brother and sister for being co-conspirators in exploration and general supporters in life. iv Acknowledgments I wish to acknowledge the numerous undergraduates that served as mentees who kept me company in the lab and aided variously in this work, including Sema Osman, Mady Herrmann, Jon Foltz, John Thundathil, Sophia Nicholas, and Keshap Poudel. Thank you to George Keeney for maintenance of the OSU Insectary Greenhouse Periplaneta americana colony. Thanks to Marymegan Daly and John Freudenstein for use of histology preparation equipment and lab space. Thanks to Leslie Jackson for use of a microscope and histology prep equipment. v Vita 1999……………………………………………………….West Muskingum High School 2003…………………………………………B.S. Biological Sciences, Cornell University 2004-2006…………………..……………………...U.S. Peace Corps, Niger, West Africa 2006-2013………………………………………………Flint Ridge Vineyard and Winery 2014-Present………...Graduate Teaching/Research Associate, The Ohio State University Publications Jahnes, B.C., Sabree, Z.L., 2020. Nutritional symbiosis and ecology of host-gut microbe systems in the Blattodea. Curr. Opin. Insect Sci. 39, 35–41. https://doi.org/10.1016/j.cois.2020.01.001 Vera-Ponce de León, A., Jahnes, B.C., Duan, J., Camuy-Vélez, L.A., Sabree, Z.L., 2020. Cultivable, Host-Specific Bacteroidetes Symbionts Exhibit Diverse Polysaccharolytic Strategies. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.00091-20 Jahnes, B.C., Herrmann, M., Sabree, Z.L., 2019. Conspecific coprophagy stimulates normal development in a germ-free model invertebrate. PeerJ 7, e6914. https://doi.org/10.7717/peerj.6914 Garrick, R.C., Sabree, Z.L., Jahnes, B.C., Oliver, J.C., 2017. Strong spatial-genetic congruence between a wood-feeding cockroach and its bacterial endosymbiont, across a topographically complex landscape. J. Biogeogr. 44, 1500–1511. https://doi.org/10.1111/jbi.12992 Thirunavukkarasu, N., Jahnes, B., Broadstock, A., Rajulu, M.B.G., Murali, T.S., Gopalan, V., Suryanarayanan, T.S., 2015. Screening marine-derived endophytic fungi for xylan-degrading enzymes. Current Science (Vol. 109). vi Fields of Study Major Field: Microbiology vii Table of Contents Abstract ............................................................................................................................... ii Dedication .......................................................................................................................... iv Acknowledgments............................................................................................................... v Vita ..................................................................................................................................... vi List of Tables ...................................................................................................................... x List of Figures .................................................................................................................... xi General Introduction ........................................................................................................... 1 Chapter 1. Nutritional symbiosis and ecology of host-microbe systems in the Blattodea. 4 ABSTRACT .................................................................................................................... 4 Gut Microbial Diversity .................................................................................................. 4 Host Insect/Microbe Interactions .................................................................................... 7 Microbe/Microbe Interactions ...................................................................................... 10 Microbial Community Assembly .................................................................................. 12 Conclusions and Future Perspectives............................................................................ 14 Chapter 2. A Low Cost and Modular System for Rearing Germ-Free and Gnotobiotic American Cockroaches (Periplaneta americana). ........................................................... 15 ABSTRACT .................................................................................................................. 15 INTRODUCTION ........................................................................................................ 16 MATERIALS AND METHODS .................................................................................. 30 RESULTS ..................................................................................................................... 38 DISCUSSION ............................................................................................................... 49 Chapter 3. Conspecific Coprophagy Stimulates Normal Development in a Germ-Free Model Invertebrate. ........................................................................................................... 55 ABSTRACT .................................................................................................................. 55 INTRODUCTION ........................................................................................................ 56 viii MATERIALS AND METHODS .................................................................................. 59 RESULTS ..................................................................................................................... 64 DISCUSSION AND CONCLUSIONS ........................................................................ 74 Chapter 4. Microbial Colonization Promotes Epithelial Expansion in Gut Subcompartments of Periplaneta americana. .................................................................. 79 ABSTRACT .................................................................................................................. 79 INTRODUCTION ........................................................................................................ 80 MATERIALS AND METHODS .................................................................................. 82 RESULTS ..................................................................................................................... 89 DISCUSSION ..............................................................................................................
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