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ABSTRACT EVANS, MATTHEW RICHARD. Global Effects of the Transcriptional Regulators ArcA and FNR in Anaerobically Grown Salmonella enterica sv. Typhimurium 14028s. (Under the direction of Dr. Hosni M. Hassan.) The purpose of this research was to assess and compare the genome-wide transcriptional profiles and virulence in mice of the global regulators, FNR (Fumarate Nitrate Reductase) and ArcA (Aerobic Respiratory Control) in anaerobically grown Salmonella enterica serovar Typhimurium 14028s. FNR controls the expression of target genes by sensing and responding to the presence or absence of dioxygen via assembly-disassembly of oxygen-liable iron-sulfur clusters, while ArcA is a two-component (ArcA/ArcB), cytosolic redox response regulator. This work demonstrates that FNR is a positive regulator of motility, flagellar biosynthesis, and pathogenesis. An fnr mutant was non- motile, lacked flagella, attenuated for virulence in mice, and did not survive inside macrophages. In S. Typhimurium, as in Escherichia coli, the FNR modulon encompassed the core metabolic and energy functions as well as motility. Salmonella-specific genes/operons regulated by FNR included those required for ethanolamine utilization, newly identified flagellar genes (mcpAC, cheV), several virulence genes in Salmonella pathogenicity island 1 (SPI-1), and the srfABC operon. ArcA serves as a transcriptional repressor/activator coordinating cellular metabolism and motility. An arcA mutant was non-motile, lacked flagella, and was as virulent as the wild-type strain via intraperitoneal challenge in mice. In S. Typhimurium, as in E. coli, the ArcA modulon encompassed the core metabolic and energy functions as well as motility. Salmonella-specific genes/operons regulated by ArcA included those for propanediol utilization, newly identified flagellar genes (mcpAC, cheV), Gifsy- 1 prophage genes, and a few virulence genes located in SPI-3 (mgtBC, slsA, STM3784). Regulation by either ArcA or FNR in S. Typhimurium is similar, but distinct from that in E. coli. Genes/operons involved in the succinyl-CoA pathway, fatty acid degradation, flagellar biosynthesis, motility, chemotaxis, cytochrome oxidase complexes are regulated similarly in the two organisms by ArcA. Genes/operons involved in aerobic metabolism, NO• detoxification, flagellar biosynthesis, motility and chemotaxis, and anaerobic carbon utilization are regulated similarly in the two organisms by FNR. Herein, we present the first report on the global role of these two redox regulators in S. Typhimurium. According this study, we hypothesize that FNR plays a more heirarchical role than ArcA in pathogenesis and during the transition between aero- and anaerobiosis in the host. Furthermore, when comparing the motility and virulence results from our work on FNR to those on ArcA, we show that the lack of motility does not necessarily correspond to the lack of virulence in S. Typhimurium. Global Effects of the Transcriptional Regulators ArcA and FNR in Anaerobically Grown Salmonella enterica sv. Typhimurium 14028s by Matthew Richard Evans A dissertation submitted to the graduate faculty of North Carolina State University In partial fulfillment of the requirements for the Degree of Doctorate of Philosophy Microbiology Raleigh, North Carolina 2008 APPROVED BY: _________________________ Dr. Craig Altier _________________________ ________________________ Dr. Matthew D. Koci Dr. Eric S. Miller _________________________ _________________________ Dr. Jonathan Olson Chair of Advisory Committee Dr. Hosni M. Hassan DEDICATION This dissertation is dedicated to my wife Mrs. Victoria Elizabeth Evans and to my friend and colleague Dr. Jose Manuel Bruno-Barcena who have stood with me during this journey. This thesis was written in memory of Mr. Thomas Richard Evans September 27, 1946 - May 13, 2003 ii BIOGRAPHY This thesis was written towards fulfilling the requirements of the degree of Doctorate of Philosophy in Microbiology. Matthew R. Evans has conducted extensive research in the areas microbiology, molecular biology, and food safety. While pursuing a Bachelor of Science degree (1999) in Food Science at the University of Delaware, Newark, DE he conducted research examining the microbial safety of fresh-cut fruits and vegetables and the efficacy of sanitizers in disinfecting contaminated fruits and vegetables at the United States Department of Agriculture (USDA) Eastern Regional Research Center (ERRC) in Wyndmoor, PA. He also performed research to determine the efficacy of anti-fungal packaging films for DuPont®. He completed his Masters of Science degree (2002) in Food Microbiology at the University of Tennessee, Knoxville, TN where his research focused on “Phenotypic Incidence and Genotypic Diversity of Listeria Isolates Recovered from Dairy Cows, Calves, and the Farm Environment.” During his Master’s program he earned a graduate student fellowship to participate in the 20th International Rapid Methods and Automation in Microbiology Workshop, Kansas State University, Manhattan, KS (July 6-14, 2000). He obtained a Doctorate of Philosophy degree in Microbiology (2008) at North Carolina State University, Raleigh, NC where his research focused on “Global Transcriptional Regulation of Metabolism and Virulence in Salmonella enterica sv. Typhimurium 14028s: Roles of the redox-sensitive transcription regulators FNR and ArcA.” During his Doctoral program he received the “Outstanding Graduate Student Teaching Assistant of the Year Award (2007).” Matt is currently a lecturer with the Biomanufacturing Training and Education Center (BTEC) at North Carolina State University and has participated in the BTEC curriculum development and teaching of courses, which include aseptic techniques, environmental monitoring, microbial detection, cGMPs, cleaning and sanitation, bioprocessing, small-scale fermentations, and reactor sampling and product analysis. He is currently an instructor for BEC(MB) 320 - Fundamentals of Microbial Cell Culture and BEC(MB) 420 - Fundamentals of Microbial Cell Bio-transformations. iii ACKNOWLEDGMENTS I would like to express my sincere appreciation to my advisor, Dr. Hosni M. Hassan for his guidance and advice, as well as his pursuit to make me a more creative and intuitive scientist during the course of my doctoral studies. I am extremely grateful to my committee members, Drs. Craig Altier, Eric S. Miller, Matthew D. Koci, and Jonathan Olson for reviewing this manuscript. I would also like to thank them for their enduring assistance, useful suggestions, and for sharing their common sense advice with me. I wish to express my love and thanks to my wife, Victoria E. Evans, whose commitment, love, words of encouragement and hard work have continually kept me motivated over the years. I want to thank my parents, Virginia Evans-Moss and the late Thomas R. Evans, my brother, Eric, and my grandmother, Mrs. Viola Hyduke, for their love support, encouragement, perspective’s on life, and for their endless support of my academic endeavors. I would like to thank my father and mother in-law, Kenneth and Rose Spier, as well as my brother and sister in-law, Robert and Melissa Parlaman and my niece, Eve Parlaman for their love and support. I have been fortunate to know and I am grateful to Drs. Jose Bruno-Barcena and Ryan C. Fink for their friendship, suggestions, support, and assistance during the past several years. I appreciate the opportunities that Dr. Gerald M. Sapers and Mr. Robert L. Miller provided me so that I could develop as a young scientist, while working at the United States Department of Agriculture (USDA) Eastern Regional Research Center (ERRC) in Wyndmoor, PA. I thank our collaborators at the University of Colorado Health Sciences Center, Drs. Andres Vazquez-Torres and Jessica Jones-Carson and at the Sidney Kimmel Cancer Center, Drs. Michael McClelland and Steffen Porwollik. I thank Dr. Philip Silverman and Ms. Robin Harris at the Department of Botany and Microbiology, University of Oklahoma for donating the Escherichia coli anti-ArcA antibodies. I wish to recognize Dr. Sue Dagher for her time, assistance, and friendship. I appreciate Valerie Knowlton for her technical support with the microscopy. I am grateful to Drs. Gabriele Gusmini and Russell Wolfinger for their assistance with the statistical analyses/SAS iv software. I value the time and assistance with the chicken macrophage studies that Dr. Matthew Koci and the members of his laboratory provided, especially Mrs. Rizwana Ali. I thank the Department of Microbiology secretarial staff, especially Mrs. Cindy Whitehead and Mr. Robert Davis, as well as Ms. Letha Young at the Biomanufacturing Training and Education Center (BTEC) for the subtle ways in which they have helped over the last several years. v TABLE OF CONTENTS CHAPTER PAGE List of Tables ....................................................................................................................... ix List of Figures ...................................................................................................................... x I. Literature Review ................................................................................................................ 1 Introduction ........................................................................................................ 2 History ........................................................................................................... 2 Physiology and Genetics ..............................................................................
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