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Bacterial Diversity and Function Within an Epigenic Cave System and Implications for Other Limestone Cave Systems

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Bacterial Diversity and Function Within an Epigenic Cave System and Implications for Other Limestone Cave Systems University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 12-2015 Bacterial diversity and function within an epigenic cave system and implications for other limestone cave systems Kathleen Merritt Brannen-Donnelly University of Tennessee - Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Biogeochemistry Commons, Environmental Microbiology and Microbial Ecology Commons, and the Geology Commons Recommended Citation Brannen-Donnelly, Kathleen Merritt, "Bacterial diversity and function within an epigenic cave system and implications for other limestone cave systems. " PhD diss., University of Tennessee, 2015. https://trace.tennessee.edu/utk_graddiss/3543 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Kathleen Merritt Brannen-Donnelly entitled "Bacterial diversity and function within an epigenic cave system and implications for other limestone cave systems." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Geology. Annette S. Engel, Major Professor We have read this dissertation and recommend its acceptance: Terry Hazen, Steven Wilhelm, Andrew Steen, Larry McKay Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Bacterial diversity and function within an epigenic cave system and implications for other limestone cave systems A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Kathleen Merritt Brannen-Donnelly December 2015 Copyright © 2015 by Kathleen Merrit Brannen-Donnelly All rights reserved. ii ACKNOWLEDGEMENTS I have had advice, assistance, and encouragement from many people during the preparation of this dissertation. I must first thank my family for insisting that a bachelor’s degree was the only path out of high school, and for all of their continued support during graduate school. I would also like to thank my husband, Brendan, for his support, because he supported my ideals of independence and equality long before we were married. Brendan knew that graduate school was the only path for me, and together we have traveled down the long and winding path that is graduate school. I would also like to thank all of the graduate students in my research group: Sarah Keenan, Brendan Headd, Terri Brown, Chanda Drennan, Caroline Dietz, Walt Doty, and Aaron Geomann. This group of students has taught me so much about science, politics, and group dynamics. They also made research more exciting, and provided many moments that I will remember forever. Thanks also to my lab manager Audrey Paterson who helped with organization of sample trips as well as assistance sampling. Besides my research group, there are many people that assisted me with cave sampling, which is not everyone’s idea of vacation time: A.J. Campion, Kevin Kissell, Jared Apuuli, and Scott Engel. Thanks to Coy Aiken and Sam Plummer, rangers at the Carter Caves State Resort Park, for access to Cascade Cave System. Also thanks to Sam Plummer for providing precipitation data. I would also like to thank several people who helped me with coding in various languages: Steve Techtmann, Hannah Woo, Junqi Yin, Drew Steen, and Mike Cheng. I would like to thank my committee members, Larry McKay, Terry Hazen, Steven Wilhelm, and Drew Steen, who helped shape my research ideas into obtainable goals. Lastly, I would like to thank my advisor Annette Summers Engel for her support. Annette inspired me to be a scientist during my undergraduate. I have had many great experiences and opportunities because of Annette’s support during both my undergraduate and graduate career. iii ABSTRACT There are approximately 48,000 known cave systems in the United States of America, with caves formed in carbonate karst terrains being the most common. Epigenic systems develop from the downward flow of meteoric water through carbonate bedrock and the solutional enlargement of interconnected subsurface conduits. Despite carbonate karst aquifers being globally extensive and important drinking water sources, microbial diversity and function are poorly understood compared to other Earth environments. After several decades of research, studies have shown that microorganisms in caves affect water quality, rates of carbonate dissolution and precipitation, and ecosystem nutrition through organic matter cycling. However, limited prior knowledge exists for the most common system, epigenic caves, regarding microbial taxonomic diversity, their metabolic capabilities, and how community function changes during and following environmental disturbances. To evaluate community development and succession, as well as potential roles in organic matter cycling, bacteria from the Cascade Cave System (CCS) in Kentucky were investigated. From geochemical and metagenomic data collected during a five-month colonization experiment, taxonomically distinct planktonic and sediment-attached bacterial communities formed along the epigenic cave stream. This represents one of the largest metagenomic studies done from any cave. Betaproteobacteria, Gammaproteobacteria, Alphaproteobacteria, and Opitutae were the most abundant groups. Planktonic bacteria pioneered sediment-attached communities, likely attributed to functional differences related to cell motility and attachment. Organic matter cycling affected exogenous heterotrophic community composition and function downstream iv because of diminished organic matter quality over time. This was reflected in significantly different abundances of genes encoding for carbohydrate and lignin degradation between habitats and depending on cave location. The ubiquity of environmental controls on bacteria functional diversity in karst is unknown because these environments have generally been left out of microbial biogeography research. In spatial meta-analyses of bacterial diversity data from global cave systems, the ubiquity of some bacteria in karst is evident. Despite evidence for undersampling and difficulties comparing sequencing technologies and strategies, some caves appear to have novel lineages while other caves have taxonomically similar communities despite being 1000s of kilometers apart. The implications are that microbes in karst (i.e., carbonate) caves around the world are functionally comparable. v TABLE OF CONTENTS Introduction ................................................................................................................... 1 Known bacterial community diversity of caves ............................................................. 8 INTRODUCTION ........................................................................................................................... 9 METHODS .................................................................................................................................. 13 Collection and analysis of open access sequences ............................................................... 13 Statistical analyses ................................................................................................................ 14 RESULTS..................................................................................................................................... 15 DISCUSSION ............................................................................................................................... 18 REFERENCES .............................................................................................................................. 22 APPENDIX I ................................................................................................................................ 26 FIGURES ................................................................................................................................. 26 TABLES ................................................................................................................................... 32 Bacterial diversity differences along an epigenic cave stream reveal evidence of community dynamics, succession, and stability ........................................................................... 40 ABSTRACT .................................................................................................................................. 41 INTRODUCTION ......................................................................................................................... 42 MATERIALS AND METHODS ...................................................................................................... 46 Site characterization ............................................................................................................. 46 Water and sediment sampling and analyses ........................................................................ 48 Fluorescence spectroscopy ..................................................................................................
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