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1 Exploring Microbial and Functional Gene Diversity EXPLORING MICROBIAL AND FUNCTIONAL GENE DIVERSITY IN MODERN MARINE THROMBOLITIC MAT COMMUNITIES By JENNIFER MARIE MOBBERLEY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2013 1 © 2013 Jennifer Marie Mobberley 2 To my parents 3 ACKNOWLEDGMENTS I would like to acknowledge my advisor, Dr. Jamie Foster, for her mentorship and guidance. Thank you for being there when I needed you and for giving me the freedom to grow as a scientist. I am grateful to my committee members, Drs. Robert Ferl, Wayne Nicholson, Eric Triplett, and Nian Wang for providing valuable suggestions and support. I would like to thank Dr. Stephanie Havemann, Steven Ahrendt, Alexandra Duscher, Artemis Louyakis, Maya Ortega, and Regine Pamphile for their technical assistance and encouragement. I would also like to acknowledge Dr. Christina Khodadad for being there to bounce ideas off of and helping keep me grounded. This research was made possible by funding from the NASA Graduate Student Researchers Project. I am also indebted to NASA Exobiology, UF Graduate Student Council, the Department of Microbiology and Cell Science, and the Davidson fund for enabling me to present my research at international and national meetings. I would like to thank Dr. Oleksandr Moskalenko at UF’s Research Computing Center for his invaluable help with my data analysis and for giving me a little extra RAM when I needed it. Steven Ahrendt and Austin Richard-Davidson fixed my codes and helped me navigate the world of scripting. None of this would have been possible without my parents, Belinda Mellon and Daniel Mobberley who have provided constant love and encouragement. Thank you for believing in me even when you had no idea what I was doing. I also appreciate the support my extended family has provided over the years. Finally, I have to thank Amy Long, David Shambaugh, Samantha Waters, and Sara Reyes for being there with unlimited support, jokes, and beverages. Thank you all for making this dissertation possible. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................. 8 LIST OF FIGURES .......................................................................................................... 9 LIST OF ABBREVIATIONS ........................................................................................... 11 ABSTRACT .................................................................................................................... 12 CHAPTER 1 LITERATURE REVIEW ........................................................................................... 14 Microbialites ............................................................................................................ 14 Community Diversity in Microbialites ....................................................................... 15 The Biogeochemistry of Carbonate Biomineralization in Microbialites .................... 23 Highborne Cay Thrombolites as Model Microbialites .............................................. 28 2 COMPARATIVE MICROBIAL DIVERSITY ANALYSES OF MODERN MARINE THROMBOLITIC MATS BY BARCODED PYROSEQUENCING ............................ 32 Introduction .............................................................................................................. 32 Materials and Methods ............................................................................................ 34 Site Description, Sample Collection, and Microscopy ....................................... 34 Molecular Identification of Cyanobacterial Isolates from the Thrombolitic Mats ............................................................................................................... 35 Generation of Barcoded 16S Ribosomal RNA Gene Libraries ......................... 37 Bioinformatic Analysis of Barcoded 16S Ribosomal RNA Gene Libraries ........ 39 Community Comparisons Between Thrombolitic Mat Types ............................ 41 Results .................................................................................................................... 42 Morphological Characterization of Thrombolitic Mat Types .............................. 42 Small Subunit rRNA Gene Diversity in Thrombolitic Mats ................................ 44 Bacterial Community Composition .................................................................... 45 Cyanobacterial Community Composition .......................................................... 48 Archaea Community Structure .......................................................................... 50 Discussion ............................................................................................................... 51 Differences in Microbial Populations Between Thrombolitic Mat Types ........... 52 Cyanobacterial Diversity in Thrombolitic Mat Communities .............................. 53 Low Diversity Of Archaea in Highborne Cay Thrombolitic Mats ....................... 55 A Model for Microbial Succession in Thrombolitic Mat Types ........................... 57 5 3 METABOLIC POTENTIAL OF LITHIFYING CYANOBACTERIA-DOMINATED THROMBOLITIC MATS ........................................................................................... 71 Introduction .............................................................................................................. 71 Materials and Methods ............................................................................................. 74 Thrombolitic Mat Sample Collection .................................................................. 74 DNA Extraction and Illumina Sequencing .......................................................... 75 Analysis of Thrombolitic Mat Metagenomes ...................................................... 75 Comparison of Thrombolite Metagenome to Other Microbial Mat Habitats ....... 76 Metabolic Profiling with Phenotypic Microarrays ............................................... 77 Results ..................................................................................................................... 78 Community Diversity Associated with Thrombolitic Mat Metagenome .............. 79 Overview of the Functional Genes of the Thrombolitic Mat Metagenome ......... 81 Comparison of Thrombolite Metagenome to Other Functional Metagenomes .. 84 Substrate Utilization Patterns Within Thrombolitic Microbial Mats .................... 85 Discussion ................................................................................................................ 87 Cyanobacterial Molecular Pathways Dominate the Thrombolite Metagenome .................................................................................................. 88 Energy Metabolisms that Influence Carbonate Precipitation in Lithifying Microbial Mats ................................................................................................ 90 Contribution of Archaea in Thrombolitic Mat Metabolic Cycling ........................ 92 Gradients of Metabolic Potential Occur Within the Depth Profile of the Thrombolitic Mat ............................................................................................. 94 4 METATRANSCRIPTOMIC SEQUENCING OF THROMBOLITIC MAT REVEALS DISTINCT SPATIAL GRADIENTS OF METABOLISMS ASSOCIATED WITH BIOLOGICALLY INDUCED MINERALIZATION .................. 113 Introduction ............................................................................................................ 113 Materials and Methods ........................................................................................... 116 Sample Collection ............................................................................................ 116 Microelectrode Oxygen Profiles ....................................................................... 116 Nucleic Acid Extraction and Purification .......................................................... 117 DNA Sequencing and Read Processing .......................................................... 118 De novo Metagenomic Assembly and Annotation ........................................... 119 Ribosomal RNA Transcript Analysis and Classification .................................. 119 Messenger RNA Analysis ................................................................................ 120 Comparisons of Thrombolite Metagenome and Metatranscriptomes to Other Microbial Ecosystems................................................................................... 121 Results and Discussion .......................................................................................... 122 Overview of Thrombolitic Mat Sequencing Libraries ....................................... 122 Active Members of the Thrombolitic Mat Community During Peak Photosynthetic Activity ................................................................................. 124 Functional Annotation of Gene Transcript Abundance Revealed Spatial Gradients of Gene Expression within the Thrombolitic Mat ......................... 127 Conclusions ........................................................................................................... 134 6 5 SUMMARY OF RESEARCH .................................................................................. 149 LIST OF REFERENCES .............................................................................................
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