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Bacterial Response to Nanoparticles at the Molecular Level a DISSERTATION SUBMITTED to the FACULTY of the UNIVERSITY of MINNESOT

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Bacterial Response to Nanoparticles at the Molecular Level a DISSERTATION SUBMITTED to the FACULTY of the UNIVERSITY of MINNESOT Bacterial Response to Nanoparticles at the Molecular Level A DISSERTATION SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY TIAN (AUTUMN) QIU IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Christy Haynes, Advisor May 2018 © Tian (Autumn) Qiu 2018 Acknowledgements I want to sincerely thank my thesis advisor, Prof. Dr. Christy Haynes, for her endless support during the past six years. I’ve probably said “thank you” a million times to her in person and in emails, but there is never enough. Her enthusiasm and optimism in science (it’s contagious!) motivate me, and as a student from a different cultural background, her dedication to building a diverse and dynamic working environment makes the group a wonderful place for working and learning. It is my honor working with Christy, and I could not have imagined having a better advisor as passionate, professional and caring as she is. I would like to thank the whole Haynes group, with whom I have had great pleasure working and being friends with. I am thankful to many Haynes people, including but not limited to: Dr. Ian Gunsolus, Dr. Melissa Maurer-Jones and Ben Meyer for guiding me when I firstly joined the group, Dr. Solaire Finkenstaedt-Quinn for colorful calendars and cat pictures, Dr. Katie Hurley, Dr. Victoria Szlag and Nathan Klein for being movie night buddies, Dr. Zhe Gao and Bo Zhi for hanging out together, Joe Buchman for always being there to help and have a laugh with, Natalie Hudson-Smith and Peter Clement for inspiring conversations, and everyone in lab for working, learning and having fun together. I would also like to thank all undergraduates that I’ve mentored for enduring me and giving me a chance to teach. The people I’ve collaborated and been friends with in the Center for Sustainable Nanotechnology are amazing. I want to thank Dr. Jared Bozich and Nicholas Niemuth for hosting me in Milwaukee multiple times. Specifically, I am extremely thankful to Prof. Dr. Rebecca Klaper, who generously hosted me in her house and guided me into the area of toxicology; she is like my second advisor and it is my honor to work with her. I also want to give my special thanks to Prof. Vivian Feng, who is a mentor, i collaborator and great friend, and kudos to her wonderful undergraduate army. I would like to thank Dr. Marco Torelli, Dr. Ariane Vartanian, Prof. Robert Hamers and Prof. Cathy Murphy in the Center for Sustainable Nanotechnology, and Dr. Andrea Carrà and Prof. Silvia Balbo at Masonic Cancer Center at University of Minnesota, without whose guidance and collaboration I would not have been able to finish my thesis. Lastly, I would like to thank Christy, Prof. Silvia Balbo, Prof. Erin Carlson and Prof. Phil Buhlmann for being on my thesis committee. Studying abroad is not easy. I want to thank my college professor and tutor, Prof. Jian Pei, for his continuous support that has started since college. I am truly grateful to all my friends who have been supporting me, especially to Yi Zhang, Xueyang Pan, Chao Li, and the girls in our SOTA a cappella group. Finally, I want to thank Minneapolis for its beautiful skyline, its (literally) breathtaking snow and its Minnesota nice. My special thanks to our tuxedo cat, Chaplin, who always surprises me with his endless energy, his big appetite and his persistence in distracting me every time I try to work from home. ii This thesis is dedicated to my parents and my grandfather, who have been supporting me in pursuing a life and a career that I want and having faith in me. I would also like to dedicate it to my fiancé, Liyang (Leon) Ma, for always standing by my side despite of the 6,286 miles and 13 (or 14) hours in between us. iii Abstract Nanotechnology has been an emerging field due to the promising properties of engineered nanomaterials, materials with at least one dimension less than 100 nanometers. With increasing application of NPs, the risk of these novel materials to environment requires thorough investigation to prevent negative impacts. NPs have enormous variety due to combinations of chemical compositions, sizes, shapes, structures and surface modifications. Building predictive models that link NP properties to biological outcomes is the key to proactive safer NP design. High-throughput toxicity screening and investigating toxicity mechanisms are the common two strategies building towards predictive models of nanotoxicity. These two strategies work together: high-throughput assays facilitate preliminary screening of potentially toxic materials for further mechanistic studies to discover biomarkers and molecular pathways of interest, which will in turn be validated on multiple materials and organisms with high-throughput screening. My thesis work combines both strategies to develop high-throughput screening assays and mechanistic understanding at different molecular levels of how an environmental bacterium, Shewanella oneidensis MR-1, responds to various NP exposures. In this work, Chapter 1 reviews recent advances in analytical nanotoxicology and identifies four key areas that would further bring the field to its maturity. Chapter 2 represents a comprehensive mechanistic study on bacteria responding to TiO2 NPs with UVA illumination. Chapter 3 uses gene expression to explore molecular response among two organisms at different trophic levels to positively and negatively charged gold NPs. Chapter 4 identifies that purification method can be one neglected source of apparent NP toxicity. A high-throughput bacterial viability assay that is free of NP interference is presented in Chapter 5. Finally, in Chapter 6, DNA damage is revealed as a toxicity mechanism for nanoscale complex metal oxide nanomaterials to bacteria. iv Table of Contents Acknowledgements ....................................................................................................... i Abstract ........................................................................................................................ iv List of Tables ................................................................................................................ ix List of Figures ............................................................................................................... x List of Schemes ........................................................................................................... xii List of Abbreviations ................................................................................................ xiii Chapter 1 Linking nanomaterial properties to biological outcomes: analytical challenges in nanotoxicology for the next decade ............................................................................... 1 1.1 Introduction ................................................................................................ 2 1.2 From correlation to causation: shifting paradigm of mechanistic approach .................................................................................................................. 6 1.3 Overcoming NP interferences in in vitro toxicity assays ......................... 12 1.4 Connecting NP interaction to biological responses at single-cell level ... 17 1.5 Real-time and in situ measurements with chemical information at nano- bio interface .......................................................................................................... 27 1.6 Conclusion ............................................................................................... 34 Chapter 2 A mechanistic study of TiO2 nanoparticle toxicity on Shewanella oneidensis MR-1 with UVA illumination: bacterial growth, riboflavin secretion, and gene expression ......... 35 2.1 Introduction .............................................................................................. 36 2.2 Materials and methods ............................................................................. 38 2.2.1 Bacteria preparation ....................................................................... 38 2.2.2 Monitoring cell growth over time .................................................. 39 2.2.3 Monitoring cell oxygen uptake ...................................................... 39 2.2.4 G6PD cytotoxicity assay for cell viability ..................................... 40 2.2.5 Intracellular ROS generation measurement ................................... 40 2.2.6 HPLC measurement of riboflavin secretion .................................. 42 2.2.7 RNA extraction .............................................................................. 42 2.2.8 qPCR and data analysis .................................................................. 43 2.3 Results ...................................................................................................... 44 2.3.1 TiO2 nanoparticle characterization ................................................. 44 2.3.2 Effect of TiO2 NPs and UV illumination on cell growth ............... 45 2.3.3 Effect of TiO2 NPs and UV illumination on cell death .................. 48 2.3.4 ROS generation affected by TiO2 NPs and UV illumination ......... 49 2.3.5 Riboflavin secretion affected by TiO2 NPs and UV illumination .. 50 2.3.6 Effect of TiO2 NPs and UV illumination of gene expression ........ 50 2.4 Discussion ................................................................................................ 52 2.4.1 Minimal inhibition of TiO2 NPs and UV illumination on S. v oneidensis growth .........................................................................................
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