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Endolithic Microbial Ecosystems Endolithic Microbial Ecosystems: Molecular Phylogenetic Composition, Ecology and Geobiology by JEFFREY JAMES WALKER B.A. Rutgers University, 1993 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Molecular, Cellular and Developmental Biology 2005 Endolithic Microbial Ecosystems: Molecular Phylogenetic Composition, Ecology and Geobiology Copyright © 2005 Jeffrey J. Walker This thesis entitled: Endolithic Microbial Ecosystems: Molecular Phylogenetic Composition, Ecology and Geobiology has been approved for the Department of Molecular, Cellular and Developmental Biology _________________________________ Norman R. Pace _________________________________ Shelley D. Copley, Committee Chair _________________________________ Kathleen J. Danna _________________________________ Ray Fall _________________________________ Kenneth S. Krauter Date _______________ The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. ! iv ABSTRACT Walker, Jeffrey James (Ph.D., Molecular, Cellular and Developmental Biology, Department of Molecular, Cellular and Developmental Biology) Endolithic Microbial Ecosystems: Molecular Phylogenetic Composition, Ecology and Geobiology Thesis directed by Professor Norman R. Pace The endolithic environment, the pore space in rocks, is a ubiquitous microbial habitat. Photosynthesis-based endolithic communities inhabit the outer millimeters to centimeters of rocks exposed to the surface. In extremely desiccated environments, such as deserts, endolithic communities are most of the extant life. Among the simplest microbial ecosystems known, endolithic communities provide a tractable model to test ecological principles, which remain untested in microbial ecology due to experimental limitations and the extraordinary diversity of microorganisms. Previous studies have suggested specific hypotheses for endolithic communities, but these have been difficult to demonstrate with traditional microbiological techniques. Consequently, this study determined the composition of select endolithic communities with cultivation-independent, ribosomal RNA-based molecular phylogenetic methods. These methods provide incisive identification of microbial constituents and ! v specific, DNA sequence information, which can be compared universally to test hypotheses about life’s ecology and evolution. Endolithic ecosystems were studied from three distinct areas: the Rocky Mountain region and Yellowstone National Park of the USA, and Shark Bay in Western Australia. Morphologically similar to endolithic communities from previous studies, Rocky Mountain communities provide insight into endolithic ecology. Novel endolithic communities were discovered in Yellowstone geothermal environments. Electron microscopic analysis indicated Yellowstone communities are subject to mineralization and fossilization. Remnants of such fossils might provide clues about ancient life analogous to those provided by fossil stromatolites, structures preserved throughout much of the ~4 billion year geological record and considered analogs of a few extant examples. Stromatolites have been popularly considered geological evidence for oxygenic photosynthesis. Here I present the first comprehensive analysis of living Shark Bay stromatolite communities. Results suggest microorganisms other than cyanobacteria dominate these communities and probably contribute to their formation. Therefore, fossil stromatolites cannot be taken alone as evidence for oxygenic photosynthesis. Phylogenetic and statistical comparison of endolithic communities from this study and a previous study of Antarctic communities help support the principle that patterns of microbial diversity are governed by similar principles observed in macro-ecological systems. Results also provide insight into geobiological processes that shape the biosphere and help us understand the history of life on Earth and possibly elsewhere in the Solar System. ! vi ACKNOWLEDGEMENTS I thank N.R. Pace, Pace Lab members and C.M. Rumbaitis-del Rio for their support and encouragement. ! vii TABLE OF CONTENTS 1. Introduction: Endolithic Ecosystems.......................................................................! 1 1.1. Endolithic ecosystems......................................................................................! 1 1.2. The molecular phylogenetic revolution............................................................! 2 1.3. The new microbial ecology..............................................................................! 3 1.4. Model ecosystems.............................................................................................! 4 1.5. Purpose of the study.........................................................................................! 5 1.6. Molecular community analysis.........................................................................! 6 1.7. Study areas........................................................................................................! 7 1.8. Previous studies................................................................................................! 9 1.9. The endolithic environment.....................................................................! 11 1.10. Colonization factors.................................................................................! 11 1.11. Water........................................................................................................! 12 1.12. Temperature..............................................................................................! 13 1.13. Light.........................................................................................................! 14 1.14. Nutrients...................................................................................................! 14 1.15. Area, rate and age of colonization...........................................................! 15 1.16. Geobiology..............................................................................................! 16 1.17. Astrobiology............................................................................................! 18 2. Phylogenetic Composition of Endolithic Ecosystems in the Rocky Mountain Region: Ecological Implications............................................................................! 19 2.1. Introduction.....................................................................................................! 19 2.2. Materials and Methods...................................................................................! 23 2.3. Site descriptions and sample collection...................................................! 23 2.4. Sample collection.....................................................................................! 25 2.5. Ribosomal RNA community analysis......................................................! 25 2.6. Statistical methods...................................................................................! 29 2.7. Microscopy..............................................................................................! 31 2.8. Accession numbers..................................................................................! 31 ! viii 2.9. Results............................................................................................................! 32 2.10. Sample representativeness.......................................................................! 33 2.11. Composition of Rocky Mountain Communities......................................! 38 2.12. Primary producers....................................................................................! 42 2.13. Consumers................................................................................................! 47 2.14. Community comparison...........................................................................! 51 2.15. Spatial variability.....................................................................................! 55 2.16. Temporal variability.................................................................................! 58 2.17. Aspect variability.....................................................................................! 58 2.18. Epilithic component.................................................................................! 59 2.19. Microscopy..............................................................................................! 60 2.20. Biomass....................................................................................................! 62 2.21.Discussion......................................................................................................! 64 2.22. Molecular community analysis................................................................! 64 2.23. Endolithic communities and ecological implications..............................! 72 2.24. Biomass and primary productivity...........................................................! 78 2.25. Biogenic alteration, weathering and global implications.........................! 82 3. Geobiology of Endolithic Communities in the Yellowstone Geothermal Environment...........................................................................................................! 84 3.1. Introduction.....................................................................................................!
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