UNIVERSITY OF CALIFORNIA, SAN DIEGO The Comparative Genomics of Salinispora and the Distribution and Abundance of Secondary Metabolite Genes in Marine Plankton A Dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Marine Biology by Kevin Matthew Penn Committee in charge: Paul R. Jensen, Chair Eric Allen Lin Chao Bradley Moore Brian Palenik Forest Rohwer 2012 Copyright Kevin Matthew Penn, 2012 All rights reserved The Dissertation of Kevin Matthew Penn is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2012 iii DEDICATION I dedicate this dissertation to my Mom Gail Penn and my Father Lawrence Penn they deserve more credit then any person could imagine. They have supported me through the good times and the bad times. They have never given up on me and they are always excited to know that I am doing well. They just want the best for me. They have encouraged my education from both a philosophical and financial point of view. I also thank my sister Heather Kalish and brother in-law Michael Kalish for providing me with support during the beginning of my academic career and introducing me to Jonathan Eisen who ended opening the door for me to an endless bounty of intellectual pursuits. iv EPIGRAPH “Nothing in Biology Makes Sense Except in the Light of Evolution” - Theodosius Dobzhansky, 1973 v TABLE OF CONTENTS SIGNATURE PAGE ..................................................................................................................................III DEDICATION .............................................................................................................................................IV EPIGRAPH ....................................................................................................................................................V TABLE OF CONTENTS ...........................................................................................................................VI LIST OF FIGURES ....................................................................................................................................IX LIST OF TABLES ......................................................................................................................................XI ACKNOWLEDGEMENTS ....................................................................................................................XIII VITA...........................................................................................................................................................XVI PUBLICATIONS......................................................................................................................................XVI FIELD OF STUDY................................................................................................................................. XVII ABSTRACT OF THE DISSERTATION ..........................................................................................XVIII CHAPTER 1: INTRODUCTION ...............................................................................................................1 MARINE BIOLOGY ........................................................................................................................................2 MICROBIAL LOOP .........................................................................................................................................3 MARINE SEDIMENT.......................................................................................................................................4 NATURAL PRODUCT DISCOVERY.................................................................................................................7 ACTINOBACTERIA.........................................................................................................................................8 SALINISPORA ..................................................................................................................................................9 HISTORY OF EVOLUTIONARY BIOLOGY ................................................................................................... 10 MICROBIAL ECOLOGY AND EVOLUTION .................................................................................................. 12 CONCLUSION.............................................................................................................................................. 13 REFERENCES .............................................................................................................................................. 14 CHAPTER 2: GENOMIC ISLANDS LINK SECONDARY METABOLISM TO FUNCTIONAL ADAPTATION IN MARINE ACTINOBACTERIA ............................................................................ 21 INTRODUCTION .......................................................................................................................................... 22 METHODS................................................................................................................................................... 24 RESULTS AND DISCUSSION........................................................................................................................ 28 CONCLUSIONS............................................................................................................................................ 36 ACKNOWLDEGEMENTS.............................................................................................................................. 36 REFERENCES .............................................................................................................................................. 37 CHAPTER 3: COMPARATIVE GENOMICS REVEALS EVIDENCE OF MARINE ADAPTATION IN SALINISPORA SPECIES........................................................................................ 58 INTRODUCTION .......................................................................................................................................... 59 METHODS................................................................................................................................................... 63 RESULTS..................................................................................................................................................... 68 vi DISCUSSION ............................................................................................................................................... 76 CONCLUSIONS............................................................................................................................................ 80 ACKNOWLEDGMENTS................................................................................................................................ 81 REFERENCES .............................................................................................................................................. 81 FIGURES ..................................................................................................................................................... 87 TABLES....................................................................................................................................................... 92 CHAPTER 4: THE ABUNDANCE AND EXPRESSION OF SECONDARY METABOLISM GENES IN MARINE PLANKTON REVEALS NEW PHYLOGENETIC DIVERSITY OF PROTISTAN LIKE KETOSYNTHASE DOMAINS.......................................................................... 102 ABSTRACT................................................................................................................................................ 102 INTRODUCTION ........................................................................................................................................ 103 METHODS................................................................................................................................................. 107 RESULTS................................................................................................................................................... 109 DISCUSSION ............................................................................................................................................. 119 CONCLUSIONS.......................................................................................................................................... 127 ACKNOWLEDGEMENTS............................................................................................................................ 129 REFERENCES ............................................................................................................................................ 130 FIGURES ................................................................................................................................................... 137 TABLES..................................................................................................................................................... 148 CHAPTER 5: CONCLUSIONS AND FUTURE PERSPECTIVES................................................ 154 REFERENCES ............................................................................................................................................ 160 APPENDIX A: GENETIC COMPLEMENTATION OF THE OBLIGATE MARINE ACTINOBACTERIUM SALINISPORA TROPICA WITH THE LARGE