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Aeromonas Hydrophila: CRITICAL ROLE of QUORUM SENSING in BACTERIAL VIRULENCE & HOST RESPONSE

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Aeromonas Hydrophila: CRITICAL ROLE of QUORUM SENSING in BACTERIAL VIRULENCE & HOST RESPONSE COMMITTEE CERTIFICATION OF APPROVED VERSION The Dissertation Committee for Bijay Kumar Khajanchi Certifies that this is the approved version of the following dissertation: EVIDENCE OF WATER TO HUMAN TRANSMISSION OF Aeromonas hydrophila: CRITICAL ROLE OF QUORUM SENSING IN BACTERIAL VIRULENCE & HOST RESPONSE Committee: Ashok K. Chopra, Ph.D., C.Sc. Johnny W. Peterson, Ph.D. Fujio Suzuki, Ph.D. Vladimir Motin, Ph.D. Vijay Pancholi, Ph.D. __________________ Dean, Graduate School EVIDENCE OF WATER TO HUMAN TRANSMISSION OF Aeromonas hydrophila: CRITICAL ROLE OF QUORUM SENSING IN BACTERIAL VIRULENCE & HOST RESPONSE by Bijay Kumar Khajanchi, B.Sc., M.Sc. Dissertation Presented to the Faculty of the University of Texas Medical Branch Graduate School of Biomedical Sciences at Galveston in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Approved by the Supervisory Committee Ashok K. Chopra, Ph.D., C.Sc. Johnny W. Peterson, Ph.D. Fujio Suzuki, Ph.D. Vladimir Motin, Ph.D. Vijay Pancholi, Ph.D. Key words: Aeromonas hydrophila, quorum sensing, AHLs, QseBC, virulence factors, biofilm formation, motility, T6SS, protease production, septicemic mouse model of infection August 2011 Galveston, Texas © 2011, Bijay Kumar Khajanchi Dedicated to the memory of my father Late Saurendra M. Khajanchi and my eldest brother Late Subrata K. Khajanchi. To my brother Biraj K. Khajanchi for his continuous support and encouragement and my wife Taslima T. Lina for always inspiring me to reach this destination. ACKNOWLEDGEMENTS I would like to express my deepest gratitude to my mentor Dr. Ashok Chopra for his continuous support, excellence guidance and providing me with an excellent research environment in the laboratory over the past five years. I would also like to thank my PhD supervisory committee members: Drs. J.W. Peterson, F. Suzuki, V. Motin and V. Pancholi, for their support and valuable advice. My special thanks to all the members of Dr. Chopra’s laboratory: Dr. J. Sha, Dr. T. Erova, Dr. E. Kozlova, S. Brackman, M. Kirtley, S. Wang and A. Bhatia, for their enormous support and for being friends to provide an enjoyable working environment. I wish to thank Dr. V.L. Popov for his expertise and assistance in using the Electron Microscope Facility. My special gratitude to the Graduate School and the Department of Microbiology and Immunology, particularly to the graduate program coordinator, Aneth Zertuche as well as all the secretarial staff for their continuous support during my graduate training. I would like to thank Drs. L. Soong, G. Klimpel, Y. Cong, J. Endsley, and A. Ben Nasr, for their suggestions towards the immunological aspects of my PhD research project. I owe my deepest gratitude to Drs. D. Niesel, R. Konig and A. Torres, for providing me crucial suggestions to develop my future career goal and to succeed in the challenging research career path. I would like to thank Ms. Mardelle Susman for editing my manuscripts. I sincerely thank all the members of the McLaughlin Endowment Fund Committee for providing me the pre-doctoral fellowship and travel awards to support my PhD project and also all the members of the general and specific scholarships committee, GSBS, UTMB for providing me several awards during my graduate training. I would like to thank my mother, sisters, and brothers. They were always there to provide me the morale support and encouraged me with their best wishes. Finally, I would like to thank my wife, Taslima Lina, for always being there to share my success and frustrations in the graduate school. iv EVIDENCE OF WATER TO HUMAN TRANSMISSION OF Aeromonas hydrophila: CRITICAL ROLE OF QUORUM SENSING IN BACTERIAL VIRULENCE & HOST RESPONSE Publication No._____________ Bijay Kumar Khajanchi, Ph.D. The University of Texas Medical Branch at Galveston, August 2011 Supervisor: Ashok K. Chopra Aeromonas hydrophila is a Gram-negative bacterium which produces a wide variety of virulence factors leading to both intestinal and extra-intestinal infections in humans. A large number of water and clinical Aeromonas isolates were molecularly finger-printed and our data provided the evidence of successful colonization and infection of humans with particular strains of certain Aeromonas species after consumption of water. Further, we delineated the role of N-acyl homoserine lactones (AHLs; autoinducer-1 [AI-1])-mediated quorum sensing (QS) in the virulence of a diarrheal isolate SSU of A. hydrophila by generating a ΔahyRI mutant. Our data suggested that AI- 1-mediated QS modulated the in vitro virulence of A. hydrophila by regulating type 6 secretion effectors, metallo-protease production, and biofilm formation. In a septicemic mouse model, the ΔahyRI mutant was also attenuated as compared to the parental strain of A. hydrophila. In addition, we demonstrated that AHLs possess immunomodulatory and protective roles and AHL pretreatment modulates innate immune response in mice and enhances their survivability during A. hydrophila infection. Further, AHL treated animals exhibited a significantly reduced bacterial load in the blood and other mouse organs, as well as various levels of cytokines/chemokines as compared to control animals. Importantly, AHL pretreatment significantly elevated neutrophil numbers in the blood, suggesting that neutrophils quickly cleared bacteria either by phagocytosis or possibly other mechanism(s) during infection. These findings coincided with the fact that neutropenic animals were more susceptible to A. hydrophila infection than normal mice. We showed that animals challenged with A. hydrophila die because of kidney and liver damage, hypoglycemia, and thrombocytopenia, and, importantly, pretreatment of animals with AHLs prevented clinical sequelae, resulting in increased survivability of mice. Finally, we identified and characterized a new two-component based QseBC/AI-3 QS system in A. hydrophila SSU by generating a ΔqseB mutant. We noted that deletion of the qseB gene attenuated bacterial virulence in a septicemic mouse model of infection, had diminished swimming and swarming motility, and the mutant bacteria formed denser biofilms when compared to the parental strain of A. hydrophila. The decrease in the virulence of A. hydrophila ∆qseB mutant correlated with reduced production of protease and the cytotoxic enterotoxin, which has associated hemolytic activity. v Table of Contents List of Tables ....................................................................................................... viii List of Figures........................................................................................................ ix INTRODUCTION 1 CHAPTER 1 5 Review of the Literature ..........................................................................................5 The Genus Aeromonas....................................................................................5 Most Common Clinical Infections Associated with Aeromonas....................6 Major Virulence Factors/Mechanisms of Aeromonas Species .....................10 Different Quorum Sensing Systems in Gram-negative Bacteria ..................16 CHAPTER 2 23 Distribution of Virulence Factors and Molecular Fingerprinting of Aeromonas Species Isolated from Water and Clinical Samples: Suggestive Evidence of Water-to-Human Transmission.....................................................................23 Introduction...................................................................................................23 Materials and Methods..................................................................................25 Results...........................................................................................................34 Discussion.....................................................................................................45 CHAPTER 3 54 N-acyl homoserine lactones involved in quorum sensing control type VI secretion system, biofilm formation, protease production, and in vivo virulence from a clinical strain of Aeromonas hydrophila.......................................................54 Introduction...................................................................................................54 Materials and Methods..................................................................................55 Results...........................................................................................................63 Discussion.....................................................................................................74 vi CHAPTER 4 82 Immunomodulatory and Protective Roles of Quorum Sensing Signaling Molecules N- acyl Homoserine Lactones during Infection of Mice with Aeromonas hydrophila .......................................................................................................................82 Introduction...................................................................................................82 Materials and Methods..................................................................................84 Results...........................................................................................................88 Discussion...................................................................................................108 CHAPTER 5 115 Two-Component QseBC System Involved in AI-3 Quorum-Sensing Regulates In Vitro and In Vivo Virulence of Aeromonas hydrophila..............................115 Introduction.................................................................................................115
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