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Comparative Phenotypic and Genomics Approaches Comparative Phenotypic and Genomics Approaches Provide Insight into the Tripartite Symbiosis of Xenorhabdus bovienii with Steinernema Nematode and Lepidopteran Insect Hosts Item Type text; Electronic Thesis Authors McMullen, John George II Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 25/09/2021 05:58:01 Link to Item http://hdl.handle.net/10150/596124 COMPARATIVE PHENOTYPIC AND GENOMICS APPROACHES PROVIDE INSIGHT INTO THE TRIPARTITE SYMBIOSIS OF XENORHABDUS BOVIENII WITH STEINERNEMA NEMATODE AND LEPIDOPTERAN INSECT HOSTS by John George McMullen II ____________________________ A Thesis Submitted to the Faculty of the SCHOOL OF ANIMAL AND COMPARATIVE BIOMEDICAL SCIENCES In Partial Fulfillment of the Requirements For the Degree of MASTER OF SCIENCE In the Graduate College THE UNIVERSITY OF ARIZONA 2015 STATEMENT BY AUTHOR This thesis has been submitted in partial fulfillment of requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library. Brief quotations from this thesis are allowable without special permission, provided that an accurate acknowledgement of the source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. SIGNED: John G. McMullen II APPROVAL BY THESIS DIRECTOR This thesis has been approved on the date shown below: January 12, 2016 S. Patricia Stock, PhD Date Department of Entomology ACKNOWLEDGMENTS Throughout my life I have had many important people to help me get to where I am today. The most influential of these people are my mother and grandmother. They have been my role models and have constantly supported me through thick and thin. Without their continued love and support, none of this would be possible. In addition to my family, I would like to thank five mentors that have been essential to my academic success. The first was my junior year high school English and Psychology teacher, Rosalyn McDermott. She taught me that the key to success in life is happiness. Without happiness, one should question the path they lead and strive to find a new route to joy. Mrs. McDermott helped me realize a hard lesson in life, that although success is important, it is more important to learn what it means to you and how you define it for yourself. Success and happiness are in the eye of the beholder. Then, my second mentor was my high school biology teacher Vanessa Montgomery. From her, I learned that I had a passion for the microscopic organisms present around us that help drive the diverse interactions in nature that allow for life to exist. Without her, I am not sure if I would have found my love for the biological sciences and in particular my fascination for protozoa. I learned from Mrs. Montgomery that you should always pursue all of your interests, and that it is always important to do what you love. I would also like to acknowledge two members of my thesis committee, Dr. Gayatri Vedantam and Dr. Fiona McCarthy who were also influential in my thought process! Dr. Vedantam helped me refine my skills of critical thinking and the scientific method. Although I have heard over and over again throughout my collegiate career what the scientific method is, I don’t think I gained a full appreciation for its power until this past year when I took MIC 595A. 3 Dr. McCarthy provided advice on omics issues and functional correlation of omic data. She changed many of my perspectives of what I do and how I approach an experiment. Lastly, Dr. S. Patricia Stock, my major advisor, is someone who has always been there for me throughout my collegiate career. In particular, she was the one who initiated me into my career as a scientist and a researcher when I was an undergraduate student. None of this research would have come to fruition without her continued encouragement. She shared with me her passion for research and guided my interests for microbial symbioses with animals. She also provided me with intellectual support and mentorship in every possible way both through my undergraduate and graduate research. I would not be where I am today if it were not for the kind, talented, empathetic, and exceptional individual that she is. I would also like to thank a few members of Dr. Stock’s laboratory who helped me in this research project. Dr. Anaïs Castagnola was a great aid in my scientific and personal development. She is a great teacher and friend who is always willing to help me to develop skills and made me question what I knew to truly gain a sense of understanding of the theories that contribute to biology. Dr. Castagnola pushed me this past year to apply for a Ph.D. program, which I am not sure I would have directly applied for another graduate program right away. Another member in Dr. Stock’s Lab is Rousel Orozco, who has also been a teacher and friend. From needing a coffee break to discuss what went wrong in my experiments to answering my endless questions on statistics, Rousel is someone who wass always ready and willing to help. Finally, I would like to thank all the other undergraduate students who helped me with the experiments and have allowed me to mentor them during their tenure in Dr. Stock’s Lab. In particular, three undergraduate students: Aidan Foster, David Jones, and Julia Muldoon-Marquez as 4 well as Alex Roder, a master’s student in the Stock lab, for their help with completing the bacterial competition assays and insect virulence assays in chapter 1. 5 TABLE OF CONTENTS LIST OF FIGURES……………………………………………………………………….8 LIST OF TABLES………………………………………………………………………...9 ABSTRACT………………………………………………………………………….….10 INTRODUCTION.……….…..…..……..…....…….……....……..……..……..….….…12 The phylum Nematoda…………………….……………….…………………….12 The family Steinernematidae…………………………………………………….16 Highlights of the genus Steinernema …………………………………………….19 Xenorhabdus symbionts………………………………………………………….19 Steinernema-Xenorhabdus lifecycle……………………………………………..21 Evolutionary origins of entomopathogeny……………………………………….24 Evolution of attenuated virulence in Xenorhabdus spp………………………….26 Fidelity and specificity in Steinernema-Xenorhabdus associations……………...28 Research objectives…………………………......………………………………..31 References………………………………………………………………………..33 CHAPTER 1: A COMPARATIVE PHENOTYPIC AND GENOMICS APPROACH TO ASSESS VARIATION IN VIRULENCE OF X. BOVIENII STRAINS………………...48 Abstract…………………………………………………………………………..50 Introduction……………………………………………………………………....51 Material and methods…………………………………………………………….53 Results…………………………………………………………………………....63 Discussion………………………………………………………………………..67 References………………………………………………………………………..75 6 Supplemental documents……………………………………………………….97 7 LIST OF FIGURES INTRODUCTION Figure 1, Steinernema phylogenetic framework (from Nadler et al ., 2006)……………..18 Figure 2, Generalized Steinernema-Xenorhabdus lifecycle (from Emelianoff et al ., 2008)……………………………………………………………………………..22 Figure 3, Simplified evolutionary scheme of insect parasitism and pathogeny in Nematoda (from Dillman et al ., 2012)…………………………………………...24 CHAPTER 1 Figure 1, Tanglegram of co-phylogeny of Xenorhabdus -Steinernema spp. used in study88 Figure 2, Schematic representation of setup for preference assays……………………...89 Figure 3, Percent gene count by COG classification of ORFs present within genomes of virulent strains……………………………………………………..……..……....90 Figure 4, Type VI secretion system in Xb SS-2004 genome (XBJ1_2096-XBJ1_2114).91 Figure 5, Bacterial competition assays………………………………………….……….92 Figure 6, Effect of T6SS + strains on T6SS - on average……………………………….…93 Figure 7, Bacterial preference assays…………………………………………………….95 Figure S1, Function of modules present and their conservation in X. bovienii genomes104 Figure S2, Nematode attraction to virulent and attenuated strains……………………..105 Figure S3, ANCOVA analysis of phylogenetic distance as co-factor for the ability of each nematode to discern between T6SS + and T6SS - strains………………………..107 8 LIST OF TABLES INTRODUCTION CHAPTER 1 Table 1, Bacterial and nematode strains used in assays and comparative genomics analyses……………………………………………………………………….….85 Table 2, LD 50 (cells/insect) of Xenorhabdus strains………………………………..……87 Table S1, Insect virulence associated ORFs present only in the genomes of consistently virulent X. bovienii strains………………………………………………….……99 Table S2, LT 50 (h) of X. bovienii strains in S. littoralis ………………………………...103 9 ABSTRACT Nematodes are highly diverse animals capable of interacting with almost every other form of life on Earth from general trophic interactions to intimate and persistent symbiotic associations. Much of their recognition originates from their various parasitic lifestyles. From an agricultural standpoint, plant parasitic nematodes are widely known for the destruction they can cause to crop plants, such as the case of the root-knot nematode Meloidogyne incognita, or livestock animals, like the Trichinella spiralis, which infects pigs and other animals.
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