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Understanding the Molecular Strategies of Campylobacter Jejuni for Survival in Amoeba and Chicken

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Understanding the Molecular Strategies of Campylobacter Jejuni for Survival in Amoeba and Chicken University of Arkansas, Fayetteville ScholarWorks@UARK Theses and Dissertations 1-2019 Understanding the Molecular Strategies of Campylobacter jejuni for Survival in Amoeba and Chicken. Deepti Pranay Samarth University of Arkansas, Fayetteville Follow this and additional works at: https://scholarworks.uark.edu/etd Part of the Food Microbiology Commons, Food Processing Commons, and the Pathogenic Microbiology Commons Recommended Citation Samarth, Deepti Pranay, "Understanding the Molecular Strategies of Campylobacter jejuni for Survival in Amoeba and Chicken." (2019). Theses and Dissertations. 3302. https://scholarworks.uark.edu/etd/3302 This Dissertation is brought to you for free and open access by ScholarWorks@UARK. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of ScholarWorks@UARK. For more information, please contact [email protected]. Understanding the Molecular Strategies of Campylobacter jejuni for Survival in Amoeba and Chicken. A dissertation submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Poultry Science by Deepti Pranay Samarth Guru Ghasidas University Bachelor of Science, 2005 RTM Nagpur University Master of Science in Microbiology, 2007 August 2019 University of Arkansas This dissertation is approved for recommendation to the Graduate Council. ___________________________________ Young Min Kwon Ph.D. Dissertation Director ___________________________________ ________________________________ Steven C. Ricke, Ph.D. Billy M. Hargis, Ph.D. Committee Member Committee Member ___________________________________ Ravi D. Barabote, Ph.D. Committee Member Abstract Campylobacter jejuni endure to be major cause of gastroenteritis in humans worldwide. C. jejuni is fastidious in laboratory setup but can cause waterborne infection through contaminated water where none of these fastidious conditions are met. This dissertation presents an assortment of studies focused in reviewing three major factors which could present a helping hand to C. jejuni in its environmental survival viz. i) association with free-living amoebae (FLA) ii) horizontal gene transfer (HGT) contributing towards its genetic diversity iii). Viable but non- culturable (VBNC) state. Acanthamoeba is a FLA linked to environmental survival of many intracellular pathogens, including C. jejuni. In Chapter-2, we studied role of 10 important C. jejuni genes in C. jejuni-Acanthamoeba interactions. Deletion mutants of these C. jejuni genes were constructed and used in internalization and 24-hrs survival assay with A. castellanii and A. polyphaga. We found that these genes are important in C. jejuni-Acanthamoeba interactions. C. jejuni benefits in transition in changing ecology by its genetic diversity largely attributed by HGT. In Chapter-3, we presented evidence of extensive HGT through homologous recombination between two C. jejuni marker strains distinguished by their chromosomally encoded antibiotic markers. We found that naked extrachromosomal DNA is an important player in contributing genetic diversity in C. jejuni. Chicken cecal supernatant was found a better recombination medium for HGT for C. jejuni. In chapter-4, whole-proteome of C. jejuni from C. jejuni-Acanthamoeba interaction was analyzed using differentially expressed proteins. Relative abundance of 404 C. jejuni proteins help us understand that in 3hrs interaction C. jejuni shifts its metabolism towards fumarate in its intracellular survival in A. castellanii. Results from chapter-2 and 4, indicate that C. jejuni has conserved mechanisms while interacting with both human and amoeba host. Inability to culture using conventional culture techniques present a major hurdle in studying C. jejuni in its VBNC state. C. jejuni transition from physiologically active to VBNC, whole-proteome comparison between samples collected at time-points between 1day and 30days was made in chapter-5. After clustering analysis by using 575 identified C. jejuni proteins, 7 clusters of proteins were identified which share a similar trend in this transition period. ©2019 by Deepti Pranay Samarth All Rights Reserved Dedication This dissertation is dedicated to My Mother – Mrs. Surekha Ramtekkar. “Mom, I can never thank enough for your love and support”. Acknowledgements This dissertation is possible through the support and encouragement of many people. It is a pleasure for me to acknowledge them before I could finish my degree. Foremost, I am sincerely thankful to Dr. Young Min Kwon, for being an excellent guide and my constant source of inspiration. I am deeply influenced by his humble nature and truly believe that my experiences in this degree program was enjoyable because I could work with him and his research group. His way of looking at scientific problems have shaped and enhanced my research perspective. I would like to thank Dr. Tieshan Jiang and all lab mates, especially Yichao Yang, Sardar Karash, Rabindra Mandal, Turki Dawoud, Bishnu Adhikari and Dr. Nicole Colhoun. I was incredibly fortunate to have the support of such amazing lab mates. I would like to express gratitude to my dissertation committee. My sincere thanks to Dr. Steven Ricke for research advice and improving my scientific writing skills. I would like to thank Dr. Billy Hargis for providing me with valuable feedback on my research and to Dr. Ravi Barabote for constructive scientific advice and insightful comments to improve my experiments. I am thankful to Department Head, Dr. Michael Kidd, Graduate Coordinator, Dr. John Marcy and all faculty members of the Department of Poultry Science. I would also like to acknowledge administrative staff, and graduate students of the Department of Poultry Science for their help and support during the course of my degree. I am also grateful to Dr. Michael Slavik and Dr. Geetha S. Kumar-Phillips for teaching me how to work with C. jejuni which help me to put a strong foundation for most experiments. I appreciated the efforts of Dr. Rohana Liyanage who helped me with the proteomic experiments. I would like to acknowledge the Department of Poultry Science for graduate assistantship provide 4 years (May 2013-May 2017) and SREB (Southern Regional Education Board) for Dissertation year fellowship. Finally, I would like to thank God for blessing me with an incredibly supportive family who motivated me in every disposition of this degree. I owe thanks to my husband, Pranay Samarth, my son Aditya, my father, Late. Khemraj D. Ramtekkar, my mother, Surekha Ramtekkar and my siblings for becoming pillars of my strength. Table of Contents Chapter 1: Introduction/Literature Review 1 1.1. Taxonomy and history of C. jejuni 2 1.2 Infection, symptoms and sequel of C.jejuni 3 1.3 Physiological characteristics of C. jejuni 5 1.4. Virulent factors of C. jejuni 6 1.5. Natural reservoirs of C. jejuni 7 1.6. Transmission of C. jejuni in poultry flock 8 1.6.1 Horizontal transmission of C. jejuni in poultry flock 8 1.6.2 Vertical transmission of C. jejuni in poultry flock 9 1.7. Role of environmental water in the transmission 10 1.8. VBNC (Viable but non-culturable) forms of C. jejuni 11 1.9. Free living amoeba- C. jejuni interactions 12 1.9.1. FLA and its role in the transmission of pathogens 13 1.9.2. Acanthamoeba - one of the most common FLA studied with C. jejuni 15 1.9.3. C. jejuni interactions with Acanthamoeba 16 1.9.4. Mechanism of C. jejuni and Acanthamoeba interaction 17 1.10. C. jejuni genetic diversity and genome plasticity 19 1.11. Horizontal gene transfer in C. jejuni 20 1.12. Objectives of the dissertation 21 1.13. References 22 Chapter 2: Genetic factors of Campylobacter jejuni required for the interaction with free- living amoebae 35 2.1. Abstract 37 2.2. Introduction 39 2.3. Material and methods 42 2.3.1. Strains and culture conditions 42 2.3.2 DNA manipulation and C. jejuni deletion mutant construction 43 2.3.3. Internalization assay 44 2.3.4. 24-hrs intracellular survival assay 46 2.3.5. Statistical analyses 47 2.4. Results 47 2.4.1. Internalization assay 48 2.3.4. 24-hrs intracellular survival assay 49 2.5. Discussion 50 2.6. References 60 2.7 Tables and figures 69 2.8 Appendix 75 2.8.1. IBC protocol 75 Chapter 3: Horizontal genetic exchange of chromosomally encoded markers between Campylobacter jejuni cells 76 3.1. Abstract 78 3.2. Introduction 80 3.3. Material and methods 82 3.3.1. Bacterial strains 82 3.3.2. Construction of marker strains of C. jejuni 83 3.3.3. Recombination assay 84 3.3.4. PCR assay to check homologous recombination 85 3.3.5. Extension of incubation time to 24 hrs 85 3.3.6. Comparison of recombination in liquid media and biphasic medium 85 3.3.7. Recombination across strain background barrier 86 3.3.8. Use of CFS to evaluate the HGT in absence of cell-to-cell contact 86 3.3.9. Recombination experiment in the presence of DNase I treatment 86 3.3.10. Detection of released C. jejuni chromosomal DNA in the culture supernatant 87 3.3.11. Chicken cecal supernatant preparation 87 3.3.12. Recombination in presence of chicken cecal supernatant 88 3.3.13. Statistical analyses 88 3.4. Results 88 3.4.1. Construction of the Marker strains 88 3.4.2. Recombination assay 89 3.4.3. PCR validating homologous recombination 89 3.4.4. Extension of incubation time to 24 hrs 90 3.4.5. Comparison of recombination in liquid media and biphasic medium 90 3.4.6. Recombination across strain background barrier 90 3.4.7. Use of CFS to evaluate HGT in absence of cell-to-cell contact 91 3.4.8. Recombination experiment in the presence of DNase I treatment 91 3.4.9. Detection of released C. jejuni chromosomal DNA in the culture supernatant 92 3.4.10. Recombination in presence of chicken cecal-supernatant 92 3.5. Discussion 93 3.6. Abbreviation 103 3.7. References 104 3.8 Tables and figures 112 3.9 Appendix 123 3.9.1.
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