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Life Histories of Bacteria: Genomic Foundations and Ecological Implications

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Life Histories of Bacteria: Genomic Foundations and Ecological Implications LIFE HISTORIES OF BACTERIA: GENOMIC FOUNDATIONS AND ECOLOGICAL IMPLICATIONS By Benjamin R. Roller A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Microbiology and Molecular Genetics – Doctor of Philosophy Ecology, Evolutionary Biology and Behavior – Dual Major 2015 ABSTRACT LIFE HISTORIES OF BACTERIA: GENOMIC FOUNDATIONS AND ECOLOGICAL IMPLICATIONS By Benjamin R. Roller Life history tradeoffs are of great interest to biologists because they are central to biodiversity theory and have the power to explain the outcomes of competition. One particular tradeoff has been a frequent target of study, the relationship between rapid and efficient reproduction. Researchers have pursued evidence for the existence of this tradeoff in many study systems and the literature surrounding this topic is extensive. While theoretical studies have indicated that a rate-efficiency tradeoff should play an important role in the evolution of bacterial populations, experiments have frequently found conflicting evidence for its existence and influence on bacterial evolution. In this dissertation I explore the physiological and ecological conditions favoring rapid and efficient bacterial growth. Microbial ecologists have long observed that the richness of cultivation medium leads to the growth of different types of bacteria. Copiotrophic bacteria have a higher relative fitness under conditions of resource abundance, while oligotrophic bacteria are favored when resources are scarce. The central topic of my dissertation research is to explore if copiotrophic bacteria employ rapid growth life history tactics and if oligotrophic bacteria employ efficient growth life history tactics. It has been noted that rapidly growing bacteria tend to possess multiple copies of the ribosomal RNA operon (rrn) in their genomes, while oligotrophic bacteria typically encode few rrn copies. I examined if rrn copy number was related to rapid and efficient growth tactics using physiological experiments and comparative genomics. The major findings from my research suggest that copiotrophs tend to utilize rapid growth tactics, while oligotrophs utilize efficient growth tactics. This evidence is consistent with a rate-efficiency tradeoff underlying divergence on this life history axis. I also demonstrate that rrn copy number is quantitative predictor of life history tactics and that it explains a large fraction of variation in the genome content of diverse bacterial species. Finally, I have explored particular features of bacterial genomes which play a role in life history adaptation. It is increasingly recognized that bacteria directly influence the health of our planet. However, the scale of bacterial diversity is immense and there is much more to learn before we can manage bacterial communities to improve wellbeing on Earth. Applying life history theory to bacteria holds promise for improving our understanding of the ecological and evolutionary forces acting on bacterial populations and communities. ACKNOWLEDGMENTS My graduate research would not have been possible without the support of many people and institutions. I am grateful to Tom Schmidt who has been a terrific mentor and PhD adviser. Not only has Tom provided intellectual and scientific guidance, but his approach to research and academic life has also been a great example to learn from. Tom’s working group has gone through many changes during my time, but the inquisitive spirit and enlightened atmosphere have been a constant source of scientific inspiration. The Schmidt lab has been a fun group of colleagues and friends to spend time with over the last seven years. I would also like to acknowledge the financial and institutional support that has helped me perform my research. The MSU graduate school, MMG department, EEBB program, Kellogg Biological Station, and U.S. Department of Energy Science Graduate Fellowship have all provided funding and the opportunity to grow as a scientist. My graduate committee has provided the guidance I needed, despite their dispersal away from East Lansing. I appreciate the extra effort Drs. Rob Britton, Jay Lennon, and Rich Lenski have contributed to help me during my graduate career. Most importantly, I would like to acknowledge my family. My parents, brothers, and in- laws have provided great encouragement over the last several years and a welcome respite from science over holidays and vacations. My wife, Alexa, has been the most supportive and encouraging partner anyone could hope for. She has helped me to become a better person and a better scientist. I have the privilege of working in a job I love, but the most exciting part of my work day is when it is over and I get to come home to her. iv TABLE OF CONTENTS LIST OF TABLES........................................................................................................................ vii LIST OF FIGURES ..................................................................................................................... viii CHAPTER 1 Life history theory provides an integrated perspective on bacterial reproduction ... 1 Introduction......................................................................................................................... 1 Life history evolution, Hutchinson’s niche, and the Bacteria............................................. 2 Physiology of bacterial reproduction.................................................................................. 5 Costs and implications of rapid bacterial growth ............................................................. 10 Summary........................................................................................................................... 12 REFERENCES ................................................................................................................. 13 CHAPTER 2 The physiology and ecological implications of efficient growth ........................... 17 Abstract............................................................................................................................. 18 Introduction....................................................................................................................... 18 When is efficient growth favored?.................................................................................... 21 Growth efficiency varies with resource availability ......................................................... 23 Growth efficiency varies with resource quality................................................................ 27 Life history and growth efficiency.................................................................................... 29 Acknowledgements........................................................................................................... 33 REFERENCES ................................................................................................................. 34 CHAPTER 3 rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development................................................................... 38 Abstract............................................................................................................................. 39 Introduction....................................................................................................................... 39 Database description ......................................................................................................... 41 Data sources...................................................................................................................... 46 Data curation..................................................................................................................... 48 Future development .......................................................................................................... 51 Acknowledgement ............................................................................................................ 51 Funding ............................................................................................................................. 51 REFERENCES ................................................................................................................. 52 CHAPTER 4 A spectrum of bacterial life history strategies are predicted by rRNA operon copy number .......................................................................................................................................... 55 Abstract............................................................................................................................. 55 Introduction....................................................................................................................... 56 Materials and Methods...................................................................................................... 59 Bacterial strains, media, and growth conditions for efficiency experiments........ 59 Maximum recorded growth rate determination .................................................... 61 Protein yield and carbon use efficiency measurements ........................................ 61 Translational power analysis................................................................................. 63 v Comparative genomic and phylogenetic analyses ................................................ 63 Statistical analyses ...............................................................................................
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