Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2010 The evolution of mitochondrial genome and proteome in animals Xiujuan Wang Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Ecology and Evolutionary Biology Commons Recommended Citation Wang, Xiujuan, "The ve olution of mitochondrial genome and proteome in animals" (2010). Graduate Theses and Dissertations. 11298. https://lib.dr.iastate.edu/etd/11298 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. The evolution of mitochondrial genome and proteome in animals by Xiujuan Wang A dissertation submitted to the graduate faculty in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Co-majors: Genetics; Bioinformatics and Computational Biology Program of Study Committee: Dennis V. Lavrov, Co-major Professor Xun Gu, Co-major Professor Karin S. Dorman Oliver Eulenstein Stephen Proulx Iowa State University Ames, Iowa 2010 ii TABLE OF CONTENTS ABSTRACT ....................................................................................................................... iv CHAPTER 1. GENERAL INTRODUCTION ....................................................................1 Introduction ......................................................................................................................1 Dissertation Organization ................................................................................................8 References ........................................................................................................................9 CHAPTER 2. MITOCHONDRIAL GENOME OF THE HOMOSCLEROMORPH OSCARELLA CARMELA (PORIFERA, DEMOSPONGIAE) REVEALS UNEXPECTED COMPLEXITY IN THE COMMON ANCESTOR OF SPONGES AND OTHER ANIMALS .................................................................................................14 Abstract ..........................................................................................................................14 Introduction ....................................................................................................................15 Materials and Methods ...................................................................................................18 Results ............................................................................................................................21 Discussion and Conclusion ............................................................................................29 Acknowledgements ........................................................................................................31 Literature Cited ..............................................................................................................32 CHAPTER 3. SEVENTEEN NEW COMPLETE MTDNA SEQUENCES REVEAL EXTENSIVE MITOCHONDRIAL GENOME EVOLUTION WITHIN THE DEMOSPONGIAE ............................................................................................................48 Abstract ..........................................................................................................................48 Introduction ....................................................................................................................49 Results ............................................................................................................................51 Discussion ......................................................................................................................60 Methods..........................................................................................................................63 Acknowledgements ........................................................................................................66 References ......................................................................................................................67 CHAPTER 4. GENE RECRUITMENT – A COMMAN MECHANISM IN THE EVOLUTION OF TRANSFER RNA GENE FAMILIES ................................................80 Abstract ..........................................................................................................................80 Introduction ....................................................................................................................81 Methods..........................................................................................................................83 Results ............................................................................................................................85 Discussion ......................................................................................................................90 Conclusion .....................................................................................................................94 Acknowledgements ........................................................................................................95 Literature Cited ..............................................................................................................96 iii CHAPTER 5. COMPARATIVE STUDY OF HUMAN MITOCHONDRIAL PROTEOME REVEALS EXTENSIVE PROTEIN SUBCELLUAR RELOCALIZATION AFTER GENE DUPLICATIONS ...............................................106 Abstract ........................................................................................................................106 Background ..................................................................................................................108 Results and Discussion ................................................................................................108 Conclusions ..................................................................................................................118 Methods........................................................................................................................119 Acknowledgements ......................................................................................................120 References ....................................................................................................................121 CHAPTER 6. GENERAL CONCLUSIONS ...................................................................133 Conclusions ..................................................................................................................133 Future Directions .........................................................................................................136 References ....................................................................................................................137 APPENDIX A. SUPPLEMENTARY MATERIALS FOR CHAPTER 2 .......................139 APPENDIX B. SUPPLEMENTARY MATERIALS FOR CHAPTER 3 .......................146 ACKNOWLEDGEMENTS .............................................................................................151 iv ABSTRACT Mitochondria, found in nearly all eukaryotes, are indispensable double membrane organelles that play pivotal roles in several cellular processes. While diversity of mitochondrial genomes among eukaryotes has been recognized, it was thought that animal mitochondrial genomes are small circular molecules with little variation in size and gene content. However this picturing of animal mitochondrial genomes was based on a biased sampling drawn primarily from bilaterian animals. In order to explore the diversity and understand the evolution of mitochondrial genomes in animals, we sequenced and analyzed mitochondrial genomes from all 14 orders of demosponges, the biggest class within sponges (phylum Porifera). Comparative genome analysis shows that a large variation in mitochondrial genome architecture is present within this group exceeding that found within Bilateria. Phylogenomic analyses based on mtDNA data support demosponges as a monophyletic group and suggest that the last common ancestor of animals might have had a tissue-level organization. Although transfer RNA (tRNA) genes are generally conserved in these genomes, evidences were found for horizontal evolution of some tRNA genes that cautioned the use of tRNA phylogeny to infer genetic code evolution. While animal mitochondrial genomes only encode a handful of proteins, the complex functions of mitochondria require over a thousand of proteins that more than 98% are nuclear encoded. Comparative gene family analyses for nuclear encoded mitochondrial proteins demonstrate that protein subcellular relocalization enabled the retention and gain of function of genes after duplications and provided a way for recruiting mitochondrial proteins. In addition, mitochondrial proteome also expanded through subfunctionalization mechanism after gene duplications. 1 CHAPTER 1. GENERAL INTRODUCTION Introduction Mitochondria, found in nearly all eukaryotes, are cellular powerhouses that produce ATP as energy source of cell through respiration/oxidative phosphorylation. They also play key roles in many other cellular processes including Krebs cycle, heme biosynthesis, cell metabolism, apoptosis, and Fe/S cluster biosynthesis. Proteins involved in these functions