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Pinpointing the Origin of Mitochondria Zhang Wang Hanchuan, Hubei

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Pinpointing the Origin of Mitochondria Zhang Wang Hanchuan, Hubei Pinpointing the origin of mitochondria Zhang Wang Hanchuan, Hubei, China B.S., Wuhan University, 2009 A Dissertation presented to the Graduate Faculty of the University of Virginia in Candidacy for the Degree of Doctor of Philosophy Department of Biology University of Virginia August, 2014 ii Abstract The explosive growth of genomic data presents both opportunities and challenges for the study of evolutionary biology, ecology and diversity. Genome-scale phylogenetic analysis (known as phylogenomics) has demonstrated its power in resolving the evolutionary tree of life and deciphering various fascinating questions regarding the origin and evolution of earth’s contemporary organisms. One of the most fundamental events in the earth’s history of life regards the origin of mitochondria. Overwhelming evidence supports the endosymbiotic theory that mitochondria originated once from a free-living α-proteobacterium that was engulfed by its host probably 2 billion years ago. However, its exact position in the tree of life remains highly debated. In particular, systematic errors including sparse taxonomic sampling, high evolutionary rate and sequence composition bias have long plagued the mitochondrial phylogenetics. This dissertation employs an integrated phylogenomic approach toward pinpointing the origin of mitochondria. By strategically sequencing 18 phylogenetically novel α-proteobacterial genomes, using a set of “well-behaved” phylogenetic markers with lower evolutionary rates and less composition bias, and applying more realistic phylogenetic models that better account for the systematic errors, the presented phylogenomic study for the first time placed the mitochondria unequivocally within the Rickettsiales order of α- proteobacteria, as a sister clade to the Rickettsiaceae and Anaplasmataceae families, all subtended by the Holosporaceae family. Using this refined mitochondrial phylogeny as framework, gene content reconstruction provides strong evidence that the last common ancestor of mitochondria and α-proteobacteria is an obligate endosymbiont possessing an iii ATP/ADP translocase that imports ATP from the host, which directly contrasts with the current role of mitochondria as the cell’s energy producer. In addition, it was predicted to possess a flagellum and be capable of oxidative phosphorylation under low oxygen condition. Our ancestral state reconstruction shines light on the driving force of the initial endosymbiosis event. We find features consistent with the “oxygen scavenger hypothesis” but no support for the alternative “hydrogen hypothesis”. Furthermore, characterization of individual bacterial genomes provides valuable insights into bacterial predation and endosymbiosis in general. iv Acknowledgement Working as a Ph.D. student has been one of the most magnificent as well as challenging experience to me. There are a great number of people without whom this research might not have been accomplished, and to whom I am greatly indebted. My first gratitude must go to my advisor, Dr. Martin Wu. It has been an honor to be his first Ph.D. student. Martin not only provided me with the opportunity to pursue my Ph.D. study in the United States, but also introduced me to the field of genomics and bioinformatics that are to become my career choice. Throughout my dissertation research, Martin has been a constant source of support both intellectually and spiritually. His guidance has been throughout every possible area of my Ph.D. research, from troubleshooting a single experiment, optimizing a Perl script, to formulating scientific ideas and the writing of this thesis. His advice has influenced me profoundly both in academic and personal level. For these, I feel so much blessed and will always be grateful. I would also like to thank all my committee members, Dr. Michael Timko, Dr. Lei Li, Dr. Cameron Mura, Dr. Douglas Taylor and Dr. Robert Cox. Their valuable inputs at each committee meeting always inspire me to think more deeply and broadly on my thesis project and the field in general. Meanwhile, I am also grateful to all the past and present lab mates. They have been making the lab an enjoyable place to work in. When I first joined lab, I knew almost nothing about programming and bioinformatics. Alex Koeppel v spent a lot of his time teaching me all the Unix basics and computational skills, without which this research could not even be started. I am also thankful to Sasha Scott, who has performed substantial preliminary work on the phylum-level bacterial phylogenetic marker database, and Tiantian Ren, who has provided many helpful suggestions to both wet bench and bioinformatic aspects of this project. This dissertation project is impossible without the considerable help from other members of UVa. I would like to especially thank John Chuckalovcak and AnhThu Nguyen from the Genomics Core Facility, who have put in many efforts generating sequencing data for this project, and Katherine Holcomb from UVACSE, who has helped me solve all kinds of technical difficulties in cluster computing. In addition, Xiaozeng Yang and Huiyong Zhang have also taught me a lot of bioinformatics and molecular biology skills that greatly facilitated the accomplishment of this project. Collaboration is an indispensable part of this project. Dr. Daniel Kadouri from UMDNJ, Dr. John Dustin Loy from University of Nebraska, and Drs. Wei Lin and Yongxin Pan from Institute of Geology and Geophysics, Chinese Academy of Sciences have all provided valuable bacterial samples and genomic DNA. Dr. Daniel Kadouri has also contributed to the manuscript preparation of the Micavibrio genome project. I would also like to thank Dr. Toni Gabaldon from CRG Barcelona who generously provided alignment data and Dr. Daniel Barker from University of St. Andrews who provided the BayesTrait program along with many helpful suggestions on the Bayesian inferences. vi Finally, I would like to express my deepest gratitude to my parents in China. My father has been my life tutor. Although he knows nothing about my research, he is always able to find a way to push me forward whenever I face difficulties. On the other hand, I have received the best care and consideration from my mother in almost every possible way. Despite being thousands of miles away, I could always feel that they are standing closely behind me. Their love has provided me with the greatest inspiration and has been driving me through the entire process. This work is dedicated to them. vii Table of Contents Abstract.............................................................................................................................. ii Acknowledgement............................................................................................................ iv Introduction....................................................................................................................... 1 References...................................................................................................................... 9 Chapter 1. A phylum level bacterial phylogenetic marker database......................... 16 Abstract........................................................................................................................ 17 Introduction................................................................................................................. 18 New Approaches.......................................................................................................... 20 Conclusion ................................................................................................................... 23 Material and Methods ................................................................................................ 24 References.................................................................................................................... 25 Chapter 2. An integrated phylogenomic approach toward pinpointing the origin of mitochondria ................................................................................................................... 40 Abstract........................................................................................................................ 41 Introduction................................................................................................................. 42 Results .......................................................................................................................... 45 Discussion .................................................................................................................... 53 Material and Methods ................................................................................................ 58 References.................................................................................................................... 64 Chapter 3. Phylogenomic reconstruction of the mitochondrial ancestors............... 108 viii Abstract...................................................................................................................... 109 Introduction............................................................................................................... 110 Results and Discussion.............................................................................................. 114 Conclusion ................................................................................................................. 130 Material and Methods .............................................................................................
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