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UC Berkeley UC Berkeley Electronic Theses and Dissertations UC Berkeley UC Berkeley Electronic Theses and Dissertations Title Spectro-Microscopic Studies of Microbial Selenium and Iron Reduction in a Metal Contaminated Aquifer Permalink https://escholarship.org/uc/item/19b6x0dr Author Fakra, Sirine Constance Publication Date 2015 Supplemental Material https://escholarship.org/uc/item/19b6x0dr#supplemental Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California Spectro-Microscopic Studies of Microbial Selenium and Iron Reduction in a Metal Contaminated Aquifer By Sirine Constance Fakra A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Earth and Planetary Science in the GRADUATE DIVISION of the UNIVERSITY OF CALIFORNIA, BERKELEY Committee in charge: Professor Jillian F. Banfield, Chair Professor James Bishop Professor Céline Pallud Spring 2015 Spectro-Microscopic Studies of Microbial Selenium and Iron Reduction in a Metal Contaminated Aquifer © 2015 By Sirine Constance Fakra Abstract Spectro-microscopic studies of microbial selenium and iron reduction in a metal contaminated aquifer by Sirine C. Fakra Doctor of Philosophy in Earth and Planetary Science University of California, Berkeley Professor Jillian F. Banfield, Chair Redox-sensitive metal contaminants in subsurface environments can be reduced enzymatically or indirectly by microbial activity to convert them from soluble mobile (toxic) to comparatively insoluble, relatively immobile (less bioavailable) forms. The broad purpose of the research presented in this dissertation was to acquire a deep understanding of selenium and iron microbial reduction and immobilization in the subsurface and to characterize in detail the nature of the bioreduction products. To this end, biofilms formed during a biostimulation experiment in a metal-contaminated aquifer adjacent to the Colorado River in Colorado, USA were studied. Biofilms develop in a wide variety of natural settings and the aqueous chemical conditions within biofilms are strongly affected by the presence of extracellular polymers that potentially confer biofilm cells with a greater tolerance to heavy metals than planktonic cells. This thesis integrates field and laboratory experimental methods to provide 2D and 3D ultrastructural information, 2D chemical speciation and community membership via metagenomics methods. In addition, physiological information was obtained via characterization of an isolated bacterium and insights related to the product structure and stability were achieved by chemical synthesis-based studies. In this dissertation, an apparatus permitting correlative cryogenic spectro-microscopy was developed (Appendix I) and applied to determine in detail the cell-mineral relationships and the speciation of selenium in the biofilms (Chapter 1). The research involved integration of both cryogenic electron microscopy and X-ray absorption spectroscopy datasets on the same sample region to document the size, structure and distribution of bioreduction products. Because many of the microbial species in the mine tailings-contaminated aquifer are novel and difficult to cultivate in the laboratory, part of the research involved phylogenic analyses of the biofilm organisms via analysis of 16S rRNA genes. A novel betaproteobacterium of the genus Dechloromonas (Dechloromonas selenatis strain RGW, Chapter 2) was isolated from the Rifle site and shown to be capable of reducing selenate to red amorphous elemental Se0. This isolate was also capable of reducing toxic arsenate. Chapter 3 investigates further the stability of elemental selenium colloids at ambient pressure as a function of temperature and particle size. The last chapter (Chapter 4) focuses on the distribution and speciation of iron in the Rifle aquifer 1 during a biostimulation experiment. The combined results demonstrate the importance of both clays and cell-associated ferric iron oxyhydroxide aggregates for growth of planktonic iron- reducing bacteria. These insights provide fundamental information about organisms that mediate selenium, iron and arsenic biogeochemical transformations in the subsurface and the nature of the product phases. The data may help to identify substrate amendment regimes for sustained Se remediation. Following short-term acetate addition to the aquifer, selenium remained immobile for at least one year, suggesting the acetate amendment approach has significant potential for bioremediation of selenium, in addition to uranium and vanadium as previously studied. Although focused on selenium and iron bio-reduction, the instrumentation and approaches developed here are generally applicable for accurate determination of cell-mineral interactions and metal speciation and can be further extended to constrain aquifer-scale reactive transport models in a wide range of environments. 2 To my brother i TABLE OF CONTENTS ACKNOWLEDGEMENTS INTRODUCTION CHAPTER 1. Correlative cryogenic spectro-microscopy to investigate selenium bioreduction products. CHAPTER 2. Dechloromonas selenatis, a Betaproteobacterium from a contaminated aquifer that reduces selenate to amorphous selenium. CHAPTER 3. Size and temperature-dependent crystallization of elemental selenium. CHAPTER 4. Iron speciation analysis indicates the use of clays and iron oxyhydroxides by planktonic- and biofilm-associated Fe-reducing bacteria. APPENDIX I. Microprobe cryogenic apparatus for correlative spectro- microscopy. APPENDIX II. Supplemental materials for Chapter 1. ii ACKNOWLEDGEMENTS As a part-time employee and graduate student, there are many people who have helped me these past years and without whom this PhD would simply not have been possible. First, to my graduate advisor Jillian Banfield who believed in me more than I did. She has been an incredible mentor. Her stimulating ideas and her vision are truly inspiring. To Howard Padmore who has made this whole journey possible, I am deeply and forever grateful. Both Jillian and Howard have supported me in more ways than I can count. I would like to thank my committee members, Jim Bishop and Céline Pallud, for taking the time to learn about my research and provide insightful feedback. I am indebted to the Advanced Light Source’s director Roger Falcone and the Berkeley Lab Learning Institute for financing me and for supporting a program where full time employees can earn a doctorate degree. I am very grateful to members of the Banfield’s group in particular Birgit Luef for teaching me the art of cryo-plunging samples and cryogenic electron microscopy, and who helped me a great deal with cryo-TEM data. I want to thank Sean Mullin, Cindy Castelle and Laura Hug who taught me the basics of microbiology and have greatly helped me with phylogenetic trees, Ken Williams for introducing me to the Rifle site and answering my tons of questions patiently. I would like to acknowledge Denise Schines for providing me with confocal data. Thanks to Roseann Csencsits, Kelly Wrighton, Luis Comolli, Kim Handley and Tyler Arbour for stimulating discussions over the years, as well as Margie Winn for administrative support. A big thanks to my Berkeley Lab colleagues, Matthew A. Marcus and Tony Warwick who always encouraged me and have been great mentors over the years; Tolek Tyliszczak, Mary K. Gilles and David K. Shuh who have always supported me; Jeff Kortright, Tony Young, Andrew Westphal and Anna Butterworth who lent me some important pieces of equipment at crucial times. A large thank you to Paul Baker and his team at Instec Inc. for help with the microprobe cryo-stage. Last, to my parents, who have always encouraged and supported me the best way they could. To my beautiful and smart brother, you are always on my mind, this one is for you. Finally to my husband, I love you so very much. I would not have made it without your unconditional love and support. iii Introduction 1.1 Introduction and motivation One of the most active current research in environmental science focuses on the bioremediation of contaminated environments. Centuries of anthropogenic activities have led to the accumulation of metal and metalloid contaminants into the environment, posing a direct threat to ecosystems and human health. By contrast to organic contaminants, heavy metals are not biodegradable and remain in the environment1. Their toxicity mostly depend on their forms, with the general rule that the more soluble they are, the more toxic2. Selenium, present in trace amounts in rock-forming minerals is a major environmental contaminant, present in the porphyry copper deposits of the western United States and around the world3. Globally, the largest fluxes in the Se cycle are from land into the marine system along aquatic pathways. Natural trace Se contamination occurs mostly through geochemical processes, such as erosion of soils and weathering of rocks (e.g. black shales)4, 5. However, the anthropogenic release is by far the major contributor to the Se cycle, releasing up to 88,000 tons of Se per year5. Oil refining, combustion of fossil fuels, drainage from mines, and agriculture represent the primary sources of contamination6. The biogeochemical cycling of selenium7, is still not well defined but is predominantly governed by microorganisms which play a crucial role in oxidation, reduction, methylation, and volatilization. Se oxyanions (selenate and selenite) which iv dominate in aqueous systems can be reduced by microbes (enzymatically, or indirectly) to comparatively insoluble, immobile and non-toxic forms (e.g.
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