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{Replace with the Title of Your Dissertation} Engineered Nanomaterial Interactions with Bacterial Cells A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCOOL OF THE UNIVERSITY OF MINNESOTA BY Ian Lyle Gunsolus IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Christy L. Haynes, Advisor May, 2016 © Ian Lyle Gunsolus 2016 Acknowledgements This dissertation is the product of many collaborations, small and large, professional and personal. Here I would like to acknowledge the generous support of all my collaborators, including professors, colleagues, friends, and family; without their support, this dissertation would not exist. First, I would like to thank my advisor, Prof. Christy Haynes, for building a research environment that helped me grow from a classroom student of chemistry to an independent researcher. By encouraging me to think beyond my independent work and actively engage with the broader scientific community, Christy has made me into a better scientist, and I thank her for it. I would also like to thank Prof. Philippe Bühlmann for his insightful contributions to my research throughout my thesis work. Through his service on my preliminary exam and thesis committees and his role as co-principal investigator (along with Christy) on research assessing the enviornmental behavior of silver nanoparticles, Phil has sharpened the focus of my research and deepened my critical analysis of chemical phenomena. My involvement in the Center for Sustainable Nanotechnology (CSN) has been a highlight of my graduate studies, and I am greatful to all past and present CSN members. I would particularly like to thank Prof. Robert Hamers, whose example of leadership through dedicated service amazes and inspires me; Prof. Joel Pedersen, who has improved my scientific reasoning and communication skills by emphasizing thorough, careful analysis and clarity of presentation; Prof. Vivian Feng, who has generously shared her perspective on research and professional development through numerous conversations; and Dr. Galya Orr and her coworkers at Pacific Northwest National Laboratory, including Drs. Dehong Hu, Craig Szymanski, and Cosmin Mihai and William Chrisler, who made my two-month research exchange both productive and enjoyable. I am grateful to the National Science Foundation’s Centers for Chemical Innovation program, which has funded the CSN under grant CHE-1503408. I have had the opportunity to work with many talented graduate students and postdocs both at the University of Minnesota and at other institutions throughout my thesis work. I would particularly like to thank Dr. Maral Mousavi, who has been a dedicated collaborator and who has modeled excellence in analytical research; Dr. Melissa Maurer- Jones, who introduced me to research in the Haynes lab and provided invaluable support in preparation for my preliminary exams; the CSN students I have most-closely collaborated with, including Mimi Hang, Drs. Kurt Jacobson and Samuel Lohse, Julianne Troiano, Marco Torelli, Dr. Thomas Kuech, Eric Melby, and Arielle Mensch; and all past and present Haynes group memebers. I have also been fortunate to mentor and work with many talented undergraduate students, including Kadir Hussein, Hilena Frew, and Lyle Nyberg. i I am grateful for the support of many staff members in the University of Minnesota Department of Chemistry, including Nancy Thao, who has answered numerous questions and provided advice to keep my graduate studies on track; Chris Lundby, who provided outstanding support during my industrial job-search; and Eric Schultz, who has helped me solve many computer and electronics issues. I am also grateful to the University of Minnesota faculty that have generously shared their resources and knowledge with me, including Prof. Kent Mann, who kindly allowed me gain research experience by working in his laboratory after I completed my undergraduate studies; and Profs. Pete Carr, Michael Sadowsky, and Michael Bowser, who, along with Profs. Christy Haynes and Philippe Bühlmann, taught my graduate courses. I would like to thank my thesis committee members not already mentioned, specifically Profs. Santiago Romero-Vargas Castrillon and Edgar Arriaga. Moreover, I am grateful to all the Professors of Chemistry at St. Olaf College who sparked my interest in the subject and provided me with a solid foundation of chemical knowledge, especially Profs. Wesley Pearson, Gary Miessler, and Jeffrey Schweinfus. I am indebted to the members of the Minneapolis Torske Klubben, who provided generous financial support during my second and third years of graduate study, and to the Univeristy of Minnesota Biotechnology Training Grant and Doctoral Dissertation Fellowship for partial funding of my research. Finally, I would like to express my deep gratitude my family. To my parents, Jeffrey and Karla Gunsolus: thank you for your devoted support throughout my journey. You have been a wellspring of knowledge, guidance, and inspiration and have made this journey possible. To my fiancée, Kirsten Petersen: thank you for enriching my life with your kindness, humor, and intelligence. You have provided me with astute perspective and continual encouragement and have made this journey possible. To my grandparents, Elton and Luella Gunsolus: thank you for your foresight and commitment to my education. You were exceptionally generous to me and have made this journey possible. ii Dedication This thesis is dedicated to all my family, friends, and colleagues. iii Abstract Nanomaterials occur naturally in a variety of forms. They exist, for example, in the aerosols produced from sea spray and in the particulates produced from incomplete combustion of hydrocarbons. In the latter 20th century, development of instruments such as the scanning tunneling microscope and atomic force microscope have allowed us to directly see and to manipulate nanoscale matter. Armed with these instrumental capabilities and a desire to push the limits of our ability to create and manipulate matter, we have begun to engineer nanomaterials for our own use. Today, nanomaterials are used as additives in numerous commercial products to improve performance and/or reduce cost. Examples include silver nanomaterials in fabrics to inhibit microbial growth and titanium dioxide nanomaterials in outdoor paints to reduce weathering. Less often, nanomaterials serve a primary function in product performance; one important example of this is the use of nanoscale mixed metal oxides as cathode materials in lithium-ion batteries, used in some electric vehicles. The increasing commercial use of engineered nanomaterials increases direct human contact with nanoscale matter beyond that which formerly occurred naturally. Taking a proactive view of these developments, a small group of researchers began, in the early 2000s, to assess the implications of nanomaterial exposure on human health, giving rise to the field of nanotoxicology. In recent years, the field has expanded its focus beyond human health to include environmental health, recognizing that the waste streams resulting from the production, use, and disposal of products containing nanomaterials serve as new sources in natural environments. The goal of environmental nanotoxicity iv research, of which my dissertation research is a part, is to promote the sustainable use of engineered nanomaterials by assessing their environmental toxicity and informing their design in order to minimize environmental impact. As a project rooted in chemistry, my dissertation focuses in particular on identifying molecular structures, both nanomaterial and biological, that can be used to predict and control the environmental impact of nanomaterials. My research focuses on characterizing the interactions of commercially relevant nanomaterials with microorganisms, which play fundamental roles in healthy ecosystems. The bacterium Shewanella oneidensis MR-1, grown in culture, was used throughout my research as a model, albeit greatly simplified, of microorganism communities in natural environments. This particular bacterium was chosen due to the worldwide distribution of its genus, Shewanella, and its ability to survive in many environments, including aerobic, anaerobic, low-temperature, and high-salinity environments. Using this drastically simplified model greatly facilitates isolation of experimental variables, which would be much more difficult to achieve in the extremely chemically complex environment of soil or water samples collected from nature. This, in turn, greatly facilitates hypothesis testing. However, experimentation using samples obtained directly from nature is also necessary to develop a complete understanding of nanomaterial behavior in the environment. My research specifically addresses the following questions: What impact does natural organic matter (a ubiquitous component of natural sediments, soils, and water bodies) have on nanoparticle toxicity to bacteria in aquatic environments? How can we visually v observe nanomaterial interactions with bacteria, both of which are near or below the diffraction limit of light, under hydrated conditions? Which structures on the bacterial cell surface primarily interact with nanomaterials? By what mechanism(s) might nanoscale battery cathode materials be toxic to bacteria, and how can we design less- toxic materials? The five major outcomes of my research, briefly summarized below, are presented in detail in Chapters 2-6. To address the first question (Chapters 2 and 3), I investigated the interactions between silver nanoparticles (also silver
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