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Identifying Ecological Differentiation in Microbial Communities Across Taxonomic Scales

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Identifying Ecological Differentiation in Microbial Communities Across Taxonomic Scales IDENTIFYING ECOLOGICAL DIFFERENTIATION IN MICROBIAL COMMUNITIES ACROSS TAXONOMIC SCALES BY NICHOLAS YOUNGBLUT DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Microbiology in the Graduate College of the University of Illinois at Urbana-Champaign, 2014 Urbana, Illinois Doctoral Committee: Associate Professor Rachel J. Whitaker, Chair Professor William W. Metcalf Professor Gary J. Olsen Professor James M. Slauch ABSTRACT Microbial diversity, both genetic and phenotypic, is a product of evolutionary and ecological processes interacting at multiple levels of biological organization. High- throughput sequencing is providing a means to resolve the vast amount of genetic diversity in microbial assemblages. However, a current fundamental challenge is associating genetic diversity, whether at the community or population scale, to phenotypic variation that defines ecological roles and dictates how microbial community diversity and ecosystem functioning respond to environmental change. In this body of work, I have used sequencing-based techniques to identify ecological differentiation at taxonomic scales ranging from a whole bacterial community to a single population of methanogenic archaea. At the broadest taxonomic scale, I used a whole-ecosystem disturbance along with 16S rRNA 454-pyrosequencing to identify ecologically relevant distinctions among taxonomic groups defined at various taxonomic scales. The findings showed that bacterial lineages require different taxonomic definitions to capture ecological patterns. At a more refined taxonomic breadth, I used a culture-independent approach to elucidate how methanogen community diversity was distributed within and between a set of freshwater lakes and also identified the ecological processes dictating this spatial distribution of diversity. Finally, at the highest resolution, I employed a comparative genomics approach to identify genomic signals of adaptive evolution in a Methanosarcina mazei population in order to link genetic variation to the ecological processes that define spatial and temporal distributions of methanogen populations. Together, this work has helped to resolve the interdependencies between genetic diversity and ecological processes, which concomitantly act to create and maintain microbial diversity across time and space. ii TABLE OF CONTENTS CHAPTER 1: INTRODUCTION ...................................................................................... 1 1.1 A MICROBIAL WORLD ................................................................................................. 1 1.2 THE IMPORTANCE OF MICROBIAL DIVERSITY .............................................................. 2 1.3 MICROBIAL COMMUNITY ASSEMBLY .......................................................................... 4 1.4 DEFINING UNITS OF DIVERSITY ................................................................................... 7 1.5 FRESHWATER LAKES: A MODEL EXPERIMENTAL SYSTEM FOR DETERMINING ECOLOGICAL DISTINCTIONS AMONG MICROBIAL CLADES ............................................... 12 1.6 THE GENETIC BASIS OF ECOLOGICAL VARIATION ...................................................... 16 1.7 METHANOSARCINA: A MODEL SYSTEM FOR DETERMINING THE GENETIC BASIS OF ECOLOGICAL VARIATION IN ARCHAEA ....................................................................... 21 1.8 OVERVIEW OF DISSERTATION ................................................................................... 25 1.9 REFERENCES ............................................................................................................ 27 CHAPTER 2: LINEAGE-SPECIFIC RESPONSES OF MICROBIAL COMMUNITIES TO A WHOLE-ECOSYSTEM DISTURBANCE ............................... 40 2.1 ABSTRACT ................................................................................................................ 40 2.2 INTRODUCTION ......................................................................................................... 41 2.3 EXPERIMENTAL PROCEDURES ................................................................................... 43 2.4 RESULTS .................................................................................................................. 48 2.5 DISCUSSION ............................................................................................................. 51 2.6 ACKNOWLEDGEMENTS ............................................................................................. 55 2.7 REFERENCES ............................................................................................................ 56 2.8 TABLES AND FIGURES ............................................................................................... 60 CHAPTER 3: DIFFERENTIATION BETWEEN SEDIMENT AND HYPOLIMNION METHANOGEN COMMUNITIES IN HUMIC LAKES .................. 68 3.1 ABSTRACT ................................................................................................................ 68 3.2 INTRODUCTION ......................................................................................................... 69 3.3 EXPERIMENTAL PROCEDURES ................................................................................... 70 3.4 RESULTS .................................................................................................................. 74 3.5 DISCUSSION ............................................................................................................. 78 iii 3.6 ACKNOWLEDGEMENTS ............................................................................................. 83 3.7 REFERENCES ............................................................................................................ 84 3.8 TABLES AND FIGURES ............................................................................................... 89 CHAPTER 4: GENOMIC DIFFERENTIATION BETWEEN TWO COEXISTING POPULATIONS OF METHANOSARCINA MAZEI ........................................................ 98 4.1 ABSTRACT ................................................................................................................ 98 4.2 INTRODUCTION ......................................................................................................... 99 4.3 EXPERIMENTAL PROCEDURES ................................................................................. 100 4.4 RESULTS ................................................................................................................ 104 4.5 DISCUSSION ........................................................................................................... 112 4.6 CONCLUSIONS ........................................................................................................ 117 4.7 ACKNOWLEDGEMENTS ........................................................................................... 117 4.8 REFERENCES .......................................................................................................... 118 4.9 TABLES AND FIGURES ............................................................................................. 123 CHAPTER 5: CONCLUDING REMARKS AND FUTURE STUDIES ...................... 132 5.1 ASSESSING ECOLOGICAL DIFFERENTIATION AT MULTIPLE SCALES OF BIOLOGICAL ORGANIZATION ........................................................................................ 132 5.2 MORE ACCURATE ASSESSMENTS OF ECOLOGICAL DIFFERENTIATION AMONG MEMBERS OF HIGHLY DIVERSE COMMUNITIES .............................................................. 133 5.3 FURTHER DEFINING THE PROCESSES OF COMMUNITY ASSEMBLY DRIVING THE SPATIOTEMPORAL DISTRIBUTION OF FRESHWATER METHANOGENS ....................... 134 5.4 LINKING GENETIC VARIATION TO ECOLOGICAL DIFFERENTIATION IN METHANOSARCINA ........................................................................................................ 135 5.5 REFERENCES .......................................................................................................... 138 APPENDIX A ................................................................................................................. 140 A.1 REFERENCES ......................................................................................................... 140 A.2 TABLES AND FIGURES ............................................................................................ 140 iv APPENDIX B ................................................................................................................. 151 B.1 TABLES AND FIGURES ............................................................................................ 151 APPENDIX C ................................................................................................................. 159 C.1 TABLES AND FIGURES ............................................................................................ 159 v CHAPTER 1: INTRODUCTION 1.1 A microbial world Microbial life is fundamental for human and global health. For ~3.7 billion of Earth’s ~4.6 billion year history, microbial life has not only persisted, but also evolved and diversified to populate every conceivable habitat, from hydrothermal vents to the surface of human skin (25,63). Bacteria and Archaea have become key players in all biogeochemical cycles by engineering a wide array of cellular machinery for conserving energy from most redox reactions thermodynamically favorable for life (41). Much of this vast array of cellular machinery has yet to be discovered and potentially adapted for industrial or
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