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University of Florida Thesis Or Dissertation Formatting CHARACTERIZING THE MOLECULAR MECHANISMS CONTRIBUTING TO BIOLOGICALLY INDUCED CARBONATE MINERALIZATION AND THROMBOLITE FORMATION By ARTEMIS S. LOUYAKIS 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 2017 © 2017 Artemis S. Louyakis To my mother, for supporting every single goal I’ve ever had, the memory of my father, for keeping me focused, and my partner, for all he’s done ACKNOWLEDGMENTS I would like to begin by acknowledging and thanking my mentor, Dr. Jamie Foster, for all her guidance throughout this Ph.D. I thank my committee members for all of their advice and support - Drs. Eric Triplett, Julie Maupin, Nian Wang, and Eric McLamore. I’d like to thank the rest of the Department of Microbiology and Cell Science, staff for always keeping my academic life in order, faculty for never turning me away when I came to use equipment or ask for help, especially Drs. K.T. Shanmugan and Wayne Nicholson, as well as Dr. Andy Schuerger from the Dept. of Plant Pathology for his advice over the years. I’d also like to acknowledge those lab members and extended lab members who made themselves readily available to talk through any problems I came up against and celebrate when all went well, including Drs. Rafael Oliveira, Jennifer Mobberley, and Giorgio Casaburi, and Lexi Duscher, Rachelle Banjawo, Maddie Vroom, Hadrien Gourlé, and so many more. I’d also like to profusely thank my family and friends who have never been anything less than completely supportive of me, specifically my partner Nathan Prince, my mother and siblings Denise Louyakis, Bobbi Louyakis, Nick Newman, Cori Sergi, extended parents and siblings Carol Prince, Barry Prince, Aaron Prince, my nieces and nephew Bailey O’Regan, Bella O’Regan, Layla Newman, Colton Prince, and Summer Prince, and my dearest friends Tina Pontbriand, Tom Pontbriand, Karen Chan, Dalal Haouchar, Alexi Casaburi, and Eloise Stikeman. Finally, I’d like to thank my funding sources for making all of this research possible: the National Science Foundation Graduate Research Fellowship Program and NASA Exobiology and Evolutionary Biology program. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 8 LIST OF FIGURES .......................................................................................................... 9 LIST OF OBJECTS ....................................................................................................... 11 LIST OF ABBREVIATIONS ........................................................................................... 12 ABSTRACT ................................................................................................................... 13 CHAPTER 1 LITERATURE REVIEW .......................................................................................... 15 Introduction to Thrombolites ................................................................................... 15 Cyanobacteria Description and Classification ......................................................... 17 Processes of Mineralization in Thrombolites ........................................................... 19 The Alkalinity Engine ........................................................................................ 21 The Role of EPS in Carbonate Precipitation ..................................................... 22 Study Site: Highborne Cay, The Bahamas ............................................................. 24 Microbial and Functional Gene Diversity In Modern Thrombolite ............................ 26 Conclusion .............................................................................................................. 30 2 A STUDY OF THE MICROBIAL SPATIAL HETEROGENEITY OF BAHAMIAN THROMBOLITES USING MOLECULAR, BIOCHEMICAL, AND STABLE ISOTOPE ANALYSES ............................................................................................ 35 Introduction ............................................................................................................. 35 Methods .................................................................................................................. 39 Sample Collection ............................................................................................ 39 Microelectrode Measurements ......................................................................... 40 Generation and Sequencing of 16S rRNA Gene Libraries ............................... 41 Bioinformatic Analysis of 16S rRNA Gene Libraries ......................................... 42 Reconstruction of Functional Metagenome Using the PICRUSt Algorithm ...... 43 Bulk Stable Isotope Analysis ............................................................................ 44 Stable Isotope Analysis Using Secondary Ion Mass Spectrometry (SIMS) ...... 45 Results .................................................................................................................... 47 Microelectrode Profiling of Thrombolite Button Mats ........................................ 47 Phylogenetic Composition of Bacteria in Thrombolite Communities with Depth ............................................................................................................ 48 Phylogenetic Composition of Archaea in Thrombolite Communities with Depth ............................................................................................................ 51 5 Spatial Profiling of Functional Gene Complexity of Thrombolite-Forming Mats Using Predictive Sequencing Analysis ................................................. 52 Stable Isotope Analyses of Thrombolitic Carbonates ....................................... 53 Discussion .............................................................................................................. 55 Microbial Diversity within Thrombolite-Forming Mats are Highly Structured ..... 55 Predictive Metagenome Reconstruction Shows Strong Correlation with Taxa and Function ........................................................................................ 59 Stable Isotope Profiling Suggests Photosynthesis is the Major Inducer of Precipitation in Thrombolite-Forming Mats .................................................... 60 Conclusion .............................................................................................................. 64 3 CHARACTERIZING THE DOMINANT CYANOBACTERIUM, DICHOTHRIX SPP., AND ITS ASSOCIATED MICROBIAL COMMUNITY USING METAGENOMIC SEQUENCING ............................................................................ 75 Introduction ............................................................................................................. 75 Materials and Methods............................................................................................ 78 Sample Collection and DNA Extraction. ........................................................... 78 Sequencing and Analysis ................................................................................. 79 Results and Discussion........................................................................................... 80 Optimizing High Quality DNA Extraction From Dichothrix spp. Filaments ........ 80 Assembly and Description of the Dominant Cyanobacteria .............................. 81 Community Associated with the Filaments ....................................................... 83 Dichothrix-Associated Cyanobacteria ........................................................ 84 Dichothrix-Associated Bacteria .................................................................. 85 Dichothrix-Associated Archaea .................................................................. 86 Functional Genes Associated with Filament Community .................................. 88 Conclusion .............................................................................................................. 91 4 A YEAR IN THE LIFE OF A THROMBOLITE: METATRANSCRIPTOME ANALYSIS OF A BAHAMIAN THROMBOLITE OVER DIEL AND SEASONAL CYCLES ............................................................................................................... 100 Introduction ........................................................................................................... 100 Materials and Methods.......................................................................................... 102 Sample Collection .......................................................................................... 102 RNA Isolation, Purification, and cDNA Synthesis ........................................... 103 Generation and Sequencing of RNA Libraries ................................................ 104 Sequence Quality Control, Assembly, Annotation, and Mapping ................... 104 Results and Discussion......................................................................................... 105 Taxonomic Dynamics within Thrombolite-Forming Button Mat Communities . 107 Metabolic Activity of the Thrombolite-Forming Community............................. 112 Differential Expression Analysis ..................................................................... 117 Thrombolite Gene Expression Network .......................................................... 119 Conclusion ...........................................................................................................
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