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The Louse Fly-Arsenophonus Arthropodicus Association

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The Louse Fly-Arsenophonus Arthropodicus Association THE LOUSE FLY-ARSENOPHONUS ARTHROPODICUS ASSOCIATION: DEVELOPMENT OF A NEW MODEL SYSTEM FOR THE STUDY OF INSECT-BACTERIAL ENDOSYMBIOSES by Kari Lyn Smith A dissertation submitted to the faculty of The University of Utah in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology The University of Utah August 2012 Copyright © Kari Lyn Smith 2012 All Rights Reserved The University of Utah Graduate School STATEMENT OF DISSERTATION APPROVAL The dissertation of Kari Lyn Smith has been approved by the following supervisory committee members: Colin Dale Chair June 18, 2012 Date Approved Dale Clayton Member June 18, 2012 Date Approved Maria-Denise Dearing Member June 18, 2012 Date Approved Jon Seger Member June 18, 2012 Date Approved Robert Weiss Member June 18, 2012 Date Approved and by Neil Vickers Chair of the Department of __________________________Biology and by Charles A. Wight, Dean of The Graduate School. ABSTRACT There are many bacteria that associate with insects in a mutualistic manner and offer their hosts distinct fitness advantages, and thus have likely played an important role in shaping the ecology and evolution of insects. Therefore, there is much interest in understanding how these relationships are initiated and maintained and the molecular mechanisms involved in this process, as well as interest in developing symbionts as platforms for paratransgenesis to combat disease transmission by insect hosts. However, this research has been hampered by having only a limited number of systems to work with, due to the difficulties in isolating and modifying bacterial symbionts in the lab. In this dissertation, I present my work in developing a recently described insect-bacterial symbiosis, that of the louse fly, Pseudolynchia canariensis, and its bacterial symbiont, Candidatus Arsenophonus arthropodicus, into a new model system with which to investigate the mechanisms and evolution of symbiosis. This included generating and analyzing the complete genome sequence of Ca. A. arthropodicus, which provided some evidence that Ca. A. arthropodicus has become recently associated with insects and may have evolved from an ancestor that was an insect pathogen. Additionally, I describe the development of methods for genetic modification of this bacterial symbiont and for introducing recombinant symbionts into louse fly hosts, as well as a new microinjection technique that enables the complete replacement of native symbionts with recombinant symbionts. With the generation of the symbiont genome sequence along with strategies for engineering recombinant symbionts and establishing them in an insect host, this work provides an interesting new system with which to investigate the function of specific genes in symbiosis as well as a promising new avenue of research involving paratransgenesis. iv TABLE OF CONTENTS ABSTRACT............................................................................................................................Ill LIST OF FIGURES............................................................................................................... vll LIST OF TABLES................................................................................................................... x Chapter 1 INTRODUCTION............................................................................................................1 References.........................................................................................................................9 2 CHARACTERISTICS OF THE COMPLETE GENOME SEQUENCE OF CANDIDATUS ARSENOPHONUS ARTHROPODICUS........................................13 Abstract............................................................................................................................13 Introductlon......................................................................................................................14 Materlals and Methods...................................................................................................16 Results and Dlscusslon...................................................................................................19 Concluslon.......................................................................................................................41 Acknowledgments..........................................................................................................43 References........................................................................................................................43 3 COMPARATIVE ANALYSIS OF THE LOUSE FLY SYMBIONT, CANDIDATUS ARSENOPHONUS ARTHROPODICUS, AND THE PARASITOID WASP SYMBIONT, ARSENOPHONUS NASONIAE...................51 Abstract............................................................................................................................51 Introductlon......................................................................................................................52 Materlals and Methods...................................................................................................55 Results and Dlscusslon...................................................................................................57 Concluslon.......................................................................................................................81 Acknowledgments..........................................................................................................84 References........................................................................................................................84 4 REPLACEMENT OF NATIVE SYMBIONTS IN THE HIPPOBOSCID LOUSE FLY, PSEUDOLYNCHIA CANARIENSIS................................................. 92 Abstract............................................................................................................................92 Introduction......................................................................................................................93 Materials and Methods...................................................................................................96 Results............................................................................................................................101 Discussion......................................................................................................................111 Acknowledgments........................................................................................................115 References......................................................................................................................116 5 CONCLUSION............................................................................................................. 120 References..................................................................................................................... 123 Appendix A ATTENUATION OF THE SENSING CAPABILITIES OF PHOQ IN TRANSITION TO OBLIGATE INSECT-BACTERIAL ASSOCIATION............124 B QUORUM SENSING PRIMES THE OXIDATIVE STRESS RESPONSE IN THE INSECT ENDOSYMBIONT, SODALIS GLOSSINIDIUS..................... 137 C PHYLOGENETIC ANALYSIS OF SYMBIONTS IN FEATHER FEEDING LICE OF THE GENUS COLUMBICOLA: EVIDENCE FOR REPEATED SYMBIONT REPLACEMENTS............................................................................... 149 vi LIST OF FIGURES Figure 2.1 Phylogenetic position of Ca. A. arthropodicus based on concatenated sequences of seven conserved orthologous genes......................................................................... 22 2.2 Plasmids of Ca. A. arthropodicus.................................................................................23 2.3 Genome features of Ca. A. arthropodicus...................................................................24 2.4 COG category classification of genes........................................................................... 27 2.5 Ribosomal RNA operon organization and heterogeneity............................................31 2.6 Gene content and organization of type III secretion system islands..........................39 3.1 BLASTCLUST analysis of intact Ca. A. arthropodicus CDSs sharing amino acid sequence identity with CDSs in A. nasoniae........................................................59 3.2 Plot of genome synteny between A. nasoniae and Ca. A. arthropodicus...................61 3.3 GC skew and positions of CDSs and pseudogenes in A. nasoniae and Ca. A. arthropodicus chromosomes.......................................................................................... 63 3.4 Average sizes of pseudogenes and intact orthologs for A. nasoniae and Ca. A. arthropodicus.................................................................................................................. 65 3.5 Monte Carlo simulation of gene inactivation in a subset of Ca. A. arthropodicus orthologs.........................................................................................................................67 3.6 The type III secretion system islands in A. nasoniae and Ca. A. arthropodicus.......76 3.7 Schematic illustrating the ymt gene in Ca. A. arthropodicus and its corresponding location in A. nasoniae......................................................................... 78 4.1 Locations of mutations in pseudogene yadhE of Ca. A. arthropodicus and the resulting yAadhE strain after lambda-Red mediated homologous recombination..102 4.2 Growth curves of yAadhE and WT strains and competitive
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