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Genomic Versatility in the Burkholderia Genus: from Strains to Species

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Genomic Versatility in the Burkholderia Genus: from Strains to Species GENOMIC VERSATILITY IN THE BURKHOLDERIA GENUS: FROM STRAINS TO SPECIES By Patrick S. G. Chain A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILSOPHY Microbiology & Molecular Genetics 2011 ABSTRACT GENOMIC VERSATILITY IN THE BURKHOLDERIA GENUS: FROM STRAINS TO SPECIES By Patrick S. G. Chain DNA sequencing has for years helped illuminate the extent of microbial diversity and their phylogenetic relationship, and more recently breathed life into most scientific disciplines, including microbiology, by allowing a complete understanding of genomic structure, functional potential, and patterns of evolution via whole genome sequencing of many species and strains. While the precise definition of bacterial species is still murky, it is clear that the group of closely related organisms classified as Burkholderia encompass a very impressive array of phenotypic properties. Using a multitude of genomic and bioinformatic methods, this thesis explores the similarities and differences at various taxonomic levels among genomes sequenced from this genus, attempts to relate some of these discoveries to other species, and discusses the implications of these findings on broader scientific questions. Pangenomic analyses among species of Burkholderia reveal an impressive array of variable genes that are not shared among all member of the genus, while comparative pangenomic analysis among strains of the same species clearly show the conservation of its main chromosome and the accelerated rate of evolution in the accessory chromosomes. A lineage-specific analysis of clinical specimens isolated over the course of 20 years reveals the evolutionary strategy for an organism highly adapted to its niche. It is clear that at all levels, the Burkholderia display remarkable genomic diversity, enabled in part by their large multi-replicon genome, and responsible for their amazing phenotypic versatility. ACKNOWLEDGMENTS I would like to extend my deep appreciation to a large number of individuals for helping me, encouraging me, and having almost forced me to both enter, and continue my graduate studies in search for this elusive PhD. I would like to begin by thanking my advisor, Professor James (Jim) Tiedje for his interest in my education and career, as my conversations with him while I was at LLNL/JGI were the spark that started me on this journey. I particularly thank him for allowing me to participate in a number of projects, and for his encouragement in pursuing new ideas and techniques. I would also like to thank the members of my committee, who were very understanding of my odd route to this PhD, and were very helpful whenever I stopped by for a chat. I am fortunate to have been introduced to so many colleagues, a fantastic array of faculty, and many outstanding scientific opportunities throughout the last several years! I would also like to thank Jim and Linda Beth for being so warm and welcoming, and have made my stays in East Lansing quite comfortable. The same is true for my friends within the Tiedje lab and within the MMG department, thank you. There are an innumerable number of friends and colleagues whose critical discussions, support, and encouragement throughout the years have helped propel me forward. I would like to specifically thank my dearest colleagues at LLNL who I call family, for without their help and encouragement, I would never have set out to pursue a PhD in this fashion. I am entirely indebted to Dr. Emilio Garcia, Victoria Lao, and members of my group who allowed me to be successful at both student and professional life. I am similarly grateful for all the support I’ve received at LANL, as my line management has been more - iii - encouraging than I could have hoped! Finally, I’d like to thank my family for their constant support, and to Krista Reitenga, who made it possible for me to finish, and continues to inspire me daily. Without the combined input and help from all of these friends and colleagues, I’m certain this adventure would have turned out quite differently. Thank you. - iv - TABLE OF CONTENTS LIST OF TABLES ..................................................................................................................... vii LIST OF FIGURES .................................................................................................................. viii CHAPTER 1 AN INTRODUCTION TO MICROBIAL GENOMICS ...................................................................... 1 Introduction .................................................................................................................... 2 Background ..................................................................................................................... 4 A perspective on microbial diversity .................................................................................. 4 The versatile Burkholderia: ultimate multi-host, multi-partner symbionts ...................... 5 Microbial genomics and sequencing technology ............................................................. 12 Bioinformatics: the next revolution ................................................................................. 17 Thesis Outline ................................................................................................................ 20 References ..................................................................................................................... 22 CHAPTER 2 GENOMES AND GENOMIC DIVERSITY WITHIN THE BURKHOLDERIA GENUS .......................... 29 Introduction .................................................................................................................. 30 Materials and Methods .................................................................................................. 35 Genomes analyzed ............................................................................................................ 35 Whole genome alignments and visualization ................................................................... 35 Ortholog identification...................................................................................................... 37 Pangenomes analysis ........................................................................................................ 37 Phylogenetic analysis ........................................................................................................ 38 Results ........................................................................................................................... 40 Inferring phylogeny of sequenced members of the Burkholderia genus ......................... 40 Whole genome alignments and genome plasticity .......................................................... 42 Burkholderia genus pangenome ....................................................................................... 44 Comparing the pangenomes of distinct lineages of Burkholderia ................................... 49 Discussion ...................................................................................................................... 53 An updated phylogeny of the Burkholderia genus ........................................................... 53 The Burkholderia genus pangenome ................................................................................ 55 The important role of species-specific genes ................................................................... 56 Differential genic content among lineages of the Burkholderia....................................... 59 Summary ........................................................................................................................... 60 References ..................................................................................................................... 62 - v - CHAPTER 3 SPECIES GENOMES AND GENOME REPRESENTATIVES: INSIGHTS FROM COMPARATIVE PANGENOMICS OF BURKHOLDERIA SPECIES ........................................................................ 69 Introduction .................................................................................................................. 70 Materials and Methods .................................................................................................. 75 Burkholderia species and strains ...................................................................................... 75 Phylogenetic tree construction ......................................................................................... 75 Whole genome alignments and visualization ................................................................... 76 Detailed comparative genomics within species ............................................................... 77 Evolutionary rate analysis ................................................................................................. 78 Core genome and pangenome analyses ........................................................................... 78 Results and Discussion ................................................................................................... 80 Whole genome alignments reveal flexible nature of species genomes ........................... 80 Detailed comparative genomics reveals a range of differences within defined species ............................................................................................................................ 84 Chromosome evolution ...................................................................................................
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