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Physiological Adaptations Contributing to Stress Survival in the Foodborne

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Physiological Adaptations Contributing to Stress Survival in the Foodborne Physiological adaptations contributing to stress survival in the foodborne pathogen Campylobacter jejuni A Thesis Presented to the Faculty of Graduate Studies of Lakehead University, Thunder Bay, Ontario by Brenda Magajna Submitted in partial fulfillment of requirements for the degree of Doctor of Philosophy in Biotechnology December 17, 2014 Brenda Magajna © 2014 PERMISSION TO USE STATEMENT In presenting this thesis in partial fulfillment of the requirements for the Doctor of Philosophy degree at Lakehead University, I agree that the Library shall make it available to use under rules of the Library. Permission for extensive quotation from or reproduction of this thesis may be granted by my major professor, or in his absence, by the Head of Biotechnology department when in the opinion of either, the proposed use of the material is for scholarly purposes. Any copying or use of the material in this thesis for financial gain shall not be allowed without my written permission. Requests for permission to copy or make other use of material in this thesis in whole or in part should be addressed to: Head of the Biotechnology Program, Lakehead University 955 Oliver Road Thunder Bay, Ontario, Canada P7B 5E1 II ABSTRACT In spite of being considered fragile and fastidious, the zoonotic pathogen Campylobacter jejuni remains the leading cause of foodborne bacterial gastroenteritis in the developed world. Lacking many of the stress responses common to other enteric pathogens, C. jejuni employs the survival strategies, biofilm formation and entry into the viable but non-culturable (VBNC) state, which have not been well characterized. Recent studies have indicated that these strategies are likely related at the molecular level. The purpose of this thesis was threefold: 1) to characterize entry into the VBNC state for planktonic and biofilm cells of C. jejuni with starvation at 4°C; 2) to evaluate a novel PMAqPCR method to quantify viable cells (both culturable and viable but non-culturable) in planktonic and biofilm cells of C. jejuni during starvation at 4°C; and 3) to investigate changes in gene expression of selected genes involved in biofilm formation and entry into the VBNC state. The three strains C. jejuni NCTC 11168 V1, C. jejuni NCTC V26 and C. jejuni 16-2R were included in all studies to compare variation based on strains. Cells were considered VBNC when there was no growth with enrichment, but cells scored as viable based on membrane integrity. Biofilm cells which became VBNC in some cases after 10 days of stress were found to enter the VBNC state earlier than planktonic cells by 10 to 50 days. Additionally, no significant reductions occurred in viable cell counts over the course of the experiments, confirming that the loss of culturability was not due to cell death (p<0.05). To date, no methods have been used to quantify viable but non-culturable biofilm cells of C. jejuni. The novel method PMAqPCR which has been successful for the enumeration of planktonic C. jejuni as well as for biofilm cells of other species was validated for quantifying C. jejuni biofilm cells in late log phase (20 h) and once cells had entered the VBNC state. The genes that affect both entry into a VBNC state and the ability to form biofilm in C. jejuni were upregulated during biofilm formation. Gene expression prior to stress treatment was 5 to 37 fold higher in biofilm cells than in their planktonic counterparts for all three strains III (p<0.001). For the planktonic samples, only one of the 3 strains showed significant changes in gene expression during the transition to the VBNC state. In this case, all 4 target genes were significantly upregulated 4-6 fold just prior to cells becoming VBNC (p<0.05). At present food and drinking water safety in Canada continues to be assessed primarily using culture-based methodology. As validated in this thesis, the ability to quantify both culturable and viable but non-culturable C. jejuni cells in both planktonic and biofilm forms will allow for improved evaluation of quality control methods in both research and industries where these pathogens are a concern. Also, the understanding of the interaction between biofilm formation and entry into the VBNC state at the molecular level described herein provides information which can be used to develop appropriate interventions and reduce the incidence of campylobacteriosis. IV Acknowledgements First and foremost I would like to thank my supervisor, Dr. Heidi Schraft for her patient guidance and support. Her mentorship has carried beyond the work presented here and has had a significant positive impact on my life in general (p<0.00001). I would also like to thank Dr. Kam Tin Leung for getting me started in the fascinating field of microbiology and for his enduring interest in my work and the work of all his students. Thank you to Dr. Neelam Khaper for serving on my committee and providing feedback on my work. Thank you also to Marc Habash who agreed to serve as my external and provide a valuable critique of my work. I am also grateful for the help provided by Misung Yim. Her technical expertise and problem solving abilities, along with her encouragement and support have been fundamental to the completion of this dissertation. There have been numerous students in the lab and in the program who have helped in a variety of ways. Thanks to all of you and best wishes on your own journeys. Thank you to all the people in the Lakehead University Instrumentation Lab (LUIL) , Al McKenzie for training on the confocal, Greg Kepka for assistance with all the everyday technical difficulties and to Ain Raitsakas for checking in to make sure I was still alive during many late nights on the confocal. This work would not have been possible without the financial support provided by both NSERC and the Ontario Graduate Scholarship program. Finally, I wish to thank my family and friends; my parents, Frank and Susan Magajna, who have been behind me in all I do in life, my children Aidan and Emily who are a constant source of inspiration and all my friends who have been supportive of my efforts here. V Table of Contents ABSTRACT ..................................................................................................................... III Acknowledgements ........................................................................................................... V Table of Contents ............................................................................................................ VI List of Tables ..................................................................................................................... X List of Figures .................................................................................................................. XI CHAPTER 1: Literature Review .................................................................................... 1 1.1 Introduction .......................................................................................................................................... 1 1.2. Campylobacter in food and water ........................................................................................................ 4 1.2.1. Poultry rearing .............................................................................................................................. 4 1.2.2. Poultry meat processing ................................................................................................................ 8 1.2.3. Campylobacter in drinking water for human consumption ........................................................ 10 1.3. Biofilms .............................................................................................................................................. 11 1.3.1. Biofilm formation on abiotic surfaces ........................................................................................ 12 1.3.2. Stages in biofilm formation ........................................................................................................ 13 1.3.3. Biofilm and epithelial tissue ....................................................................................................... 18 1.3.4. Conditions relevant to biofilm formation ................................................................................... 19 1.3.5. Strain variation ........................................................................................................................... 23 1.3.5.1. Cell surface hydrophobicity ................................................................................................ 23 1.3.5.2. Polysaccharides ................................................................................................................... 23 1.3.5.3. Source .................................................................................................................................. 24 1.3.6. Commonly used C. jejuni strains ................................................................................................ 24 1.3.7. Extended survival and stress protection of C. jejuni within biofilms ......................................... 27 1.4 The viable but non-culturable (VBNC) state ....................................................................................... 29 1.4.1. Induction of VBNC..................................................................................................................... 30 1.4.1.1. Low nutrient stress (starvation) ..........................................................................................
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