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Literature Review: Thermal Environments and Biodiversity

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GEOMICROBIOLOGICAL DESCRIPTION OF TWO CONTEMPORARY HYDROTHERMAL POOLS IN UZON CALDERA, KAMCHATKA, RUSSIA, AS MODELS FOR SULFUR BIOGEOCHEMISTRY by ELIZABETH ADRIENNE BURGESS (Under the Direction of Juergen Wiegel) ABSTRACT The combination of geological activity and geographic isolation make Uzon Caldera, Kamchatka, Russia, an ideal location for geomicrobiological research. Two hydrothermal pools, Arkashin Shurf (Arkashin) and Zavarzin Spring (Zavarzin), were selected for geochemical and microbiological characterization over multiple years and scales. Arkashin has high arsenic concentrations relative to Zavarzin, which has abundant elemental sulfur. Grab samples were analyzed from a geomicrobiological perspective, to describe community structure in each pool based on sequence, lipid and stable isotope data. Based on sequence analysis and lipid distribution, Arkashin was inhabited by Hydrogenobaculum- related primary producers. Other community members included Desulfurella-, ―Sphingobacteria―- and Variovorax-related microorganisms. Zavarzin was dominated by Chloroflexus, and heterotrophic microorganisms, including some Crenarchaeota. The community in Zavarzin was more diverse than in Arkashin. Additionally, nearly 20% of the sequences from Arkashin and over 50% of the sequences from Zavarzin represented uncultured and unclassified microorganisms. Core sample analyses indicated that in each pool the microbiology and geochemistry changed with depth over visible changes in color and texture. Surface sub-samples were similar to the grab samples. Autotrophic surface communities were replaced with microorganisms dependent on heterotrophic inputs or reduced hydrothermal carbon as depth increased. In Arkashin, variation in color of strata was associated with varying concentrations of As and S. The highest As and S concentrations were associated with the lowest concentrations of phospholipid fatty acids (PLFA). In Zavarzin, the highest sulfur and PLFA concentrations were associated with fine-textured surface samples. The patterns observed indicate the biomass and composition of microbial communities can shift considerably in association with macroscopically visible changes in geochemical conditions. The described geomicrobiological data represent sulfur biogeochemistry under distinct geochemical conditions. As- and S-concentrations are linked significantly in Arkashin. The microorganisms in Arkashin play a role in As-S cycling, in part through sulfate- reduction. In Zavarzin, elemental sulfur is abundant and sulfide from sulfate-reduction is a minor component of total sulfur concentrations. Cataloging the diversity and distribution of microorganisms in contemporary thermal environments and elucidating some of the variations that occur with depth at the edges of hydrothermal pools add to knowledge about the intersection of geochemistry and microbiology. INDEX WORDS: arsenic, thermophiles, microecology GEOMICROBIOLOGICAL DESCRIPTION OF TWO CONTEMPORARY HYDROTHERMAL POOLS IN UZON CALDERA, KAMCHATKA, RUSSIA, AS MODELS FOR SULFUR BIOGEOCHEMISTRY by ELIZABETH ADRIENNE BURGESS B.S., Stephen F. Austin State University, 1999 M.S., University of Georgia, 2003 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2009 © 2009 Elizabeth Adrienne Burgess All Rights Reserved GEOMICROBIOLOGICAL DESCRIPTION OF TWO CONTEMPORARY HYDROTHERMAL POOLS IN UZON CALDERA, KAMCHATKA, RUSSIA, AS MODELS FOR SULFUR BIOGEOCHEMISTRY by ELIZABETH ADRIENNE BURGESS Major Professor: Juergen Wiegel Committee: Gary L. Mills Samantha B. Joye William B. Whitman Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia December 2009 DEDICATION Dedication is what it has taken to get to this point. Not just my own dedication but also the dedication of all those in my life who have shared the goal. I know my husband, Jeremy Rogers, will be glad to call me doctor at last. My parents, Rich and Carole Burgess, have worked hard to get me here. My father especially has been a constant source of encouragement and advice. I would also like to dedicate this dissertation to those who have always been dedicated to me just as I am; Rafinesque, Penelope, Minazuki, Jack, and especially Okefenokee. To represent my aspirations with this work, here is a short poem: Sublimation In my quest to exalt sulfur, as it precipitates from hot and watery depths, may I also be purified from vapor into a solid form. iv ACKNOWLEDGEMENTS First and foremost I would like to acknowledge my major professor, J. Wiegel, and my committee members past and present, S. B. Joye, W. B. Whitman, G. L. Mills and A. L. Neal. Thank you for the opportunity and guidance. I would also like thank my co-authors for guidance; J. M. Unrine, V. Samarkin, D. Crowe, and C. S. Romanek. Technical help was provided by D. Addis, J. Cox, O. Tsyusko, C. Hagen, L. Dueck, T. Tuberville, N. Kabengi, H. Brant, N. Ethridge, J. Seaman, J. Singer, T. C. Glenn, J. Fiser, T. Maddox, C. Lasher. I am also grateful to my friends and fellow students C. Brooks, M. Hodges, I. Wagner, M. Wright, K. Bowers, all of my Micro Department cohort, especially N. Mesbah, T. Rogers and D. Cook; participants of the Kamchatka field expeditions, especially my fellow graduate students; our Russian colleagues, especially T. Sokolova, E.A. Bonch-Osmolovskaya, and N. Pimenov; and the Microbiology Department and Savannah River Ecology Laboratory support staff. This research was funded the National Science Foundation (NSF-MCB0238607 – Kamchatka Microbial Observatory and NSF-MCB99-77886 – Mono Lake Microbial Observatory), the U.S. Civilian Research and Devlopment Foundation, and the Savannah River Ecology Laboratory through the U.S. Department of Energy (DE-FC-09-075R22506) and the University of Georgia. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .......................................................................................................................... v LIST OF TABLES ...................................................................................................................................... vii LIST OF FIGURES ................................................................................................................................... viii CHAPTER 1 LITERATURE REVIEW: THERMAL ENVIRONMENTS AND BIODIVERSITY ............. 1 2 INTRODUCTION: UZON CALDERA, AN OVERVIEW WITH ADDITIONAL DESCRIPTION OF TWO POOLS .................................................................................... 45 3 COMPARATIVE GEOCHEMICAL AND MICROBIOLOGICAL CHARACTERIZATION OF TWO THERMAL POOLS IN THE UZON CALDERA, KAMCHATKA, RUSSIA . 63 4 VARIATION WITH DEPTH IN ELEMENTAL COMPOSITION AND MICROBIAL COMMUNITIES IN CORE SAMPLES FROM TWO THERMAL POOLS IN THE UZON CALDERA, KAMCHATKA, RUSSIA ............................................................... 110 5 EVIDENCE FOR SULFATE-REDUCTION AND BIOGENIC SULFIDE MINERALIZATION IN CORE SAMPLES FROM TWO THERMAL POOLS IN UZON CALDERA, KAMCHATKA, RUSSIA ........................................................................... 136 CONCLUSIONS....................................................................................................................................... 172 APPENDICES A A SUMMARY OF ENRICHMENT AND ISOLATION EXPERIMENTS ......................... 174 B A TIMELINE OF ENRICHMENT AND ISOLATION EXPERIMENTS ........................... 183 C MEDIA & METHODS USED IN ENRICHMENT AND ISOLATION EXPERIMENTS . 193 vi LIST OF TABLES Page Table 1.1 Comparison of richness of restriction enzyme phylotypes (types) from clone libraries of environmental 16S rRNA genes from a small selection of thermal environments ................... 42 Table 2.1 Type-strain isolates from Uzon Caldera ..................................................................................... 59 Table 3.1 Summary of data [for grab samples] ........................................................................................... 94 Table 4.1 Sub-sample depths, color, water content, and sediment chemistry for core samples ............... 128 Table 4.2 PLFA concentration, recovery and diversity in 2006 core samples .......................................... 129 Table 4.3 Sub-sample depths, percent composition and stable isotope δ-values for C and N .................. 130 Table 5.1 Sub-sample depths, color, water content, texture, sediment chemistry, and S content and stable isotope δ-values for core samples ........................................................................................... 159 Table 5.2 Sub-sample depths and pore water chemistry for core samples ............................................... 160 Table A.1 Some examples of arsenate and/or sulfate reducing prokaryotes in isolation .......................... 179 Table A.2 Ranges of estimated numbers of sulfate-reducing prokaryotes in Arkashin and Zavarzin by medium treatment (values are per 0.5 mL of sample). ........................................................... 180 vii LIST OF FIGURES Page Figure 1.1 Thermophilic archaea: aerobic/microaerophilic/facultative aerobic archaea (o) and anaerobic/facultative aerobic archaea (■). A, P. oshimae and P. torridus: optimal growth at pH 0.7, 60°C (Schleper et al., 1995). B, P. fumarii: optimal growth at 106°C, pH 5.5 (Blochl et al., 1997). C, Thermococcus acidaminovorans: optimal growth at pH 9, 85°C (Dirmeier et al., 1998). .......................................................................................................................................
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