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Constraining the Interpretation of 2-Methylhopanoids Through Genetic and Phylogenetic Methods

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Constraining the Interpretation of 2-Methylhopanoids Through Genetic and Phylogenetic Methods Constraining the interpretation of 2-methylhopanoids through genetic and phylogenetic methods Thesis by Jessica Nicole Ricci In Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy CALIFORNIA INSTITUTE OF TECHNOLOGY Pasadena, California 2015 (Defended May 21, 2015) ii © 2015 Jessica Nicole Ricci All Rights Reserved iii ACKNOWLEDGEMENTS There are many people I would like to thank for their support during my time as a graduate student. Firstly, I am grateful to my Ph.D. advisor Dianne Newman for allowing me to join her lab and for her helpful advice over the last five years. I have interacted with many wonderful people in the Newman lab who have helped me with my research enormously, especially Gargi, Chia, Dave, Caj, Alice, Megan, Suzanne, Nick, and Elise. I would also like to thank my committee members Paul Sternberg, Alex Sessions, Sarkis Mazmanian, and Jared Leadbetter for their useful advice and suggestions. A special thanks goes to Woodward Fischer, Victoria Orphan, and members of their labs for many valuable and stimulating discussions. My experience at Caltech has been enriched by a number of teaching-related activities. Thank you to Cassandra, Tina, Noelle, and Daniel. I have appreciated the countless seminars, workshops, and events you have organized that have without a doubt made me a better teacher. I am particularly grateful to Ryan Skophammer, who showed me that teaching K-12 is not a scary as I thought it would be. Lastly, I would like to thank my family for always encouraging me to pursue my interests. Mom, Dad, and John Paul, thank you for supporting me during my graduate career and beyond. To my partner, Alan, without your unwavering encouragement this would not have been possible. Thank you to my cat, Oscar, who I can always count on to greet me with lots of purring after a long day. iv ABSTRACT Hopanoids are a class of sterol-like lipids produced by select bacteria. Their preservation in the rock record for billions of years as fossilized hopanes lends them geological significance. Much of the structural diversity present in this class of molecules, which likely underpins important biological functions, is lost during fossilization. Yet, one type of modification that persists during preservation is methylation at C-2. The resulting 2-methylhopanoids are prominent molecular fossils and have an intriguing pattern over time, exhibiting increases in abundance associated with Ocean Anoxic Events during the Phanerozoic. This thesis uses diverse methods to address what the presence of 2- methylhopanes tells us about the microbial life and environmental conditions of their ancient depositional settings. Through an environmental survey of hpnP, the gene encoding the C-2 hopanoid methylase, we found that many different taxa are capable of producing 2- methylhopanoids in more diverse modern environments than expected. This study also revealed that hpnP is significantly overrepresented in organisms that are plant symbionts, in environments associated with plants, and with metabolisms that support plant-microbe interactions; collectively, these correlations provide a clue about the biological importance of 2-methylhopanoids. Phylogenetic reconstruction of the evolutionary history of hpnP revealed that 2-methylhopanoid production arose in the Alphaproteobacteria, indicating that the origin of these molecules is younger than originally thought. Additionally, we took genetic approach to understand the role of 2- methylhopanoids in Cyanobacteria using the filamentous symbiotic Nostoc punctiforme. We found that hopanoids likely aid in rigidifying the cell membrane but do not appear to provide resistance to osmotic or outer membrane stressors, as has been shown in other organisms. The work presented in this thesis supports previous findings that 2-methylhopanoids are not biomarkers for oxygenic photosynthesis and provides new insights by defining their distribution in modern environments, identifying their evolutionary origin, and investigating their role in Cyanobacteria. These efforts in modern settings aid the formation of a robust interpretation of 2-methylhopanes in the rock record. v TABLE OF CONTENTS Acknowledgements ........................................................................................................ iii Abstract ........................................................................................................................... iv Table of Contents ............................................................................................................ v List of Figures ................................................................................................................ vi List of Tables ................................................................................................................. vii Preface: Overview of Chapters ....................................................................................... 1 Chapter I: Interpreting hopanoids as molecular fossils .................................................. 3 Fossil types ............................................................................................................... 3 Introduction to hopanoids and 2-methylhopanoids ................................................. 5 Proposed interpretations of hopanoids and 2-methyhopanoids ............................... 7 Questions addressed in this thesis .......................................................................... 13 References .............................................................................................................. 14 Chapter II: Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche ............................................................................................... 22 Abstract ................................................................................................................... 22 Introduction ............................................................................................................ 23 Methods .................................................................................................................. 25 Results and Discussion ........................................................................................... 32 Acknowledgements ................................................................................................ 42 References .............................................................................................................. 44 Chapter III: Phylogenetic analysis of HpnP reveals the origin of 2-methylhopanoid production in Alphaproteobacteria ............................................................................... 51 Abstract ................................................................................................................... 51 Introduction ............................................................................................................ 52 Methods .................................................................................................................. 54 Results ..................................................................................................................... 60 Discussion ............................................................................................................... 69 Acknowledgements ................................................................................................ 74 References .............................................................................................................. 75 Chapter IV: The role of hopanoids and 2-methylhopanoids in Nostoc punctiforme ... 81 Introduction ............................................................................................................ 81 Methods .................................................................................................................. 84 Results and Discussion ........................................................................................... 87 Acknowledgements .............................................................................................. 101 References ............................................................................................................ 102 Chapter V: Conclusions and Future Directions .......................................................... 107 Conclusions .......................................................................................................... 107 Future Directions .................................................................................................. 108 Appendix A: Datasets from Chapter II ....................................................................... 112 Appendix B: Dataset from Chapter III ....................................................................... 145 vi LIST OF FIGURES Chapter I Figure 1.1 | Timeline of select geological events and oldest biomarker fossils discussed in the text ............................................................................................ 4 Figure 1.2 | Structures of select hopanoids found in extant organisms, modern environments, and ancient sedimentary depositions ......................................... 6 Figure 1.3 | Quantification of 2-methylhopanoids in specific membranes of N. punctiforme ................................................................................................. 12 Chapter II Figure 2.1 | Distribution of hpnP in cyanobacteria ...............................................
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