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ABSTRACT DUTTA, VIKRANT. Characterization of Disinfectant And ABSTRACT DUTTA, VIKRANT. Characterization of Disinfectant and Phage Resistance Determinants of Listeria monocytogenes . (Under the direction of Dr. Sophia Kathariou). Environmental contamination of food plays a key role in transmission of Listeria monocytogenes . Adaptations such as ability to grow under refrigeration, biofilm formation, disinfectant resistance, and resistance to phage are crucial to the survival of L. monocytogenes in the environment. Here we have investigated some of the adaptations that may contribute towards environmental persistence of this pathogen. These include disinfectant (quaternary ammonium compounds, QAC) resistance, temperature-dependent resistance to phage among epidemic clone II strains, triphenylmethane dye reduction and resistance to heavy metals such as cadmium. Using in silico analysis, we have analyzed the prevalence of cadAC efflux systems associated with cadmium resistance among different Listeria genomes. Of the three distinct cadAC types known to date in L. monocytogenes , two ( cadA1C1 and cadA2C2 ) were harbored by plasmids and were encountered in diverse strains of L. monocytogenes and (in the case of cadA2C2 ) non-pathogenic Listeria spp. Large plasmids from two different epidemic- associated strains of L. monocytogenes harbored cadA2C2 together with a drug efflux system (bcrABC ), and both determinants were associated with a putative IS 1216 transposon. Plasmid-cured derivatives of these strains were susceptible both to cadmium and to BC. Genetic analyses revealed that cadA2C2 was sufficient for restoring resistance to cadmium to a plasmid-cured derivative of L. monocytogenes H7550. Furthermore, bcrABC was sufficient for restoring resistance to high levels of QAC to the plasmid-cured strain. The transcription of bcrABC was temperature-dependent, with higher transcript levels at 37°C than at 25°C or below. The bcrABC system was encountered among L. monocytogenes strains of different serotypes, origin (environmental or clinical) and genotypes and was detected more frequently in strains harboring the cadmium resistance cassette cadA2C2 (alone or together with cadA1C1 ) than in those harboring cadA1C1 alone. bcrABC was found in several different genetic arrangements, mostly on plasmids, but we also identified L. monocytogenes strains in which bcrABC appeared to have translocated into the chromosome. Transcriptional analysis revealed that transcription of cadA2C2 and bcrABC was independent, and induced upon exposure to the respective compounds (cadmium and BC, respectively). On the other hand, bcrABC was co-transcribed with the downstream gene tmr , encoding a putative triphenylmethane reductase. We showed that tmr mediated decolorization (reduction) of toxic dyes such as crystal violet (CV) and that CV could also induce bcrABC . Analysis of a panel of strains of diverse serotypes revealed that those harboring tmr tended to also harbor bcrABC and cadA2C2 (alone or together with cadA1C1 ), suggesting the presence of a co-selected multi-resistance unit that includes cadA2C2 , bcrABC , and tmr . In previous studies, a gene (ORF 2753) was found to be responsible for the ability of L. monocytogenes epidemic clone II (ECII) to be resistant to phage when propagated at temperatures <25°C. Here we have shown that ORF2753 corresponded to a putative restriction endonuclease that was a component of a type II restriction-modification (RM) system (LmoH1) that is specific for GTATCC (N6/5). This RM system is present on a chromosomal genomic region unique to ECII strains. Transcriptional analysis revealed that the putative restriction endonuclease was expressed significantly more at ≤25°C than at 37°C, potentially accounting for the temperature-dependent phage resistance of ECII strains, while ORF2754 (putative methyltransferase) was expressed at all tested temperatures; this was in agreement with the resistance of the DNA from cells grown at either 25°C or 37°C to BfuI, specific for GTATCC (N6/5). Given that genetic basis for distinct adaptive attributes were elucidated in an outbreak strain (H7550), it would be of further interest to investigate the contribution of these determinants towards virulence of this pathogen. Such details would provide new avenues to control the incidence of listeriosis. Characterization of Disinfectant and Phage Resistance Determinants of Listeria monocytogenes by Vikrant Dutta A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Microbiology Raleigh, North Carolina 2011 APPROVED BY: _______________________________ ______________________________ Sophia Kathariou James Brown Committee Chair _______________________________ ______________________________ Amy Grunden Ilenys Muñiz Pérez-Díaz ii DEDICATION I would like to dedicate this dissertation to my grandmother Tara Devi Dutta whose unconditional love, values, and vision have been and will be a sole source of inspiration throughout my life. iii BIOGRAPHY Vikrant Dutta was born in the Western state of Rajasthan, India. He completed his high school in the Himalayan city Shimla in the state Himachal Pradesh, India. After completing high school, he joined Nagpur Veterinary College, Nagpur in the central Indian state of Maharashtra. After receiving degree in Veterinary Medicine, Vikrant worked as a veterinarian for a short duration in a small and large animal clinic at Nagpur before joining University of Arkansas, Fayetteville for his M.S. in Poultry Science. During M.S., his research was focused on analyzing the effects of stress and colibacillosis on the isolation of Listeria monocytogenes from synovial tissue of turkey poults. After receiving his degree from University of Arkansas in 2008, Vikrant joined the laboratory of Dr. Sophia Kathariou at North Carolina State University, Raleigh for PhD. His doctorate work at NC State has been focused on identifying and characterizing the conditions and molecular determinants responsible for environmental persistence in Listeria monocytogenes . iv ACKNOWLEDGMENTS I am forever grateful to Dr. Sophia Kathariou for believing in me and providing me with the opportunity to pursue a Ph.D. Her vision to see her students succeed and to learn from every opportunity is the driving force behind the success of our research group. For me, the tenacity of the challenges that were put forth by her during my Ph.D. has created exceptional confidence in me as a researcher. I believe attributes such as objectivity and articulate thinking that I have developed during my stay in Dr. Kathariou’s lab, will help me overcome future challenges in life. Her distinctive enthusiasm for science and never ending appetite for knowledge is phenomenal and I can only imagine living by these values. I am appreciative of all the help and valuable advice from all my committee members. I am also thankful to Robin Siletzky for her phenomenal support. Her ability to find solutions even when the odds are stacked high has been a great inspiration. I would also like to thank Dr. Driss Elhanafi whose extraordinary support was essential to my research work. His willingness to help at all times was phenomenal. The support and encouragement from all my lab mates has been great. I would also like to extend my appreciation to the great Ghazal singers especially Jagjit Singh (died Oct’2011) who have often helped me get by long and tiring days. Last but not the least; I would like to thank my family in India and my forever supportive fiancée (Ashley Stephens) for their love, encouragement and faith in my abilities. My family and especially Ashley have been a great source of strength that has helped me to persevere through the challenges. I consider myself blessed to be surrounded by a loving and caring family. v TABLE OF CONTENTS LIST OF TABLES ………………………………………………………………vii LIST OF FIGURES …………………………….…………………………….….ix CHAPTER I- LITERATURE REVIEW……………………………………….1 CHAPTER II- Genetic Characterization of Plasmid Associated Benzalkonium Chloride Resistance Determinants in a Strain of Listeria monocytogenes from the 1998-1999 Outbreak………………………………………………………...………….…….56 Abstract……………………………………………………………………57 Introduction………………………………………………………………..57 Materials and Methods…………………………………………………….59 Results………………………………………………………………….….65 Discussion…………………………………………………………………72 References…………………………………………………………………78 CHAPTER III- Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes…………........... .........98 Abstract………………………………………………………….…….......99 Introduction.………………………………………………….………. .......99 Materials and Methods.………………………………….………………..101 Results …………………………………………………….…………..........103 Discussion…..………………………………………….……………….... .103 References……………………………………………………………........109 CHAPTER IV: A Novel Restriction- Modification System is Responsible for Temperature- Dependant Phage Resistance in Listeria monocytogenes ECII………………………………………………………………………….…....127 Abstract…………………………………………………….……………...128 Introduction…………………………………………………. ………….....128 Materials and Methods…………………………………….……………....130 Results……………………………………………………………….. .......136 Discussion……………………………………………………………….....142 References…………………………………………………….………..…..147 vi CHAPTER V- Tetrahymena-conditioned Medium Promotes Survival of Listeria monocytogenes……………………………………………………………..……..169 Abstract…………………………………………………………..……..…170 Introduction……………………………………………………... ……......170 Materials and Methods…………………………………………..….….….173 Results…………………………………………………………..…..….....175
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