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Investigation of the Pseudomonas Chlororaphis PA23 - Acanthamoeba Castellanii Interaction

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Investigation of the Pseudomonas Chlororaphis PA23 - Acanthamoeba Castellanii Interaction Investigation of the Pseudomonas chlororaphis PA23 - Acanthamoeba castellanii interaction and the role of polyhydroxyalkanoates in PA23 physiology By Akrm Saleh Ghergab A Thesis Submitted to the Faculty of Graduate Studies of The University of Manitoba in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Department of Microbiology University of Manitoba Winnipeg Copyright © 2020 by Akrm Saleh Ghergab I Abstract Pseudomonas chlororaphis PA23 is a biocontrol agent (BCA) that is able to protect canola against the pathogenic fungus Sclerotinia sclerotiorum. PA23 secretes a number of metabolites that contribute to fungal antagonism, including pyrrolnitrin (PRN), phenazine (PHZ), hydrogen cyanide (HCN) and degradative enzymes. Beyond pathogen suppression, the success of a BCA is dependent upon its ability to persist in the environment and avoid the threat of grazing predators, including protozoa. The first part of this thesis investigated whether PA23 is able to resist predation by Acanthamoeba castellanii (Ac) and defined the role of antifungal (AF) compounds in the bacterial-protozoan interaction. We discovered that PRN, PHZ and HCN contribute to PA23 toxicity towards Ac trophozoites. Ac preferentially migrated towards regulatory mutants devoid of AF metabolites as well as a PRN biosynthetic mutant, indicating that AF metabolites act to repel Ac. We also discovered that toxin-producing strains were able to survive inside trophozoites for up to 24 h. Collectively, our findings indicate that PRN, PHZ and HCN are involved in amoebicidal activity, and through the production of these molecules, PA23 is able to avoid the threat of predation. PA23 accumulates polyhydroxyalkanoate (PHA) polymers as carbon and energy storage compounds. The second part of this thesis aimed to elucidate the role of PHAs in PA23 stress resistance and interaction with Ac. Three PHA biosynthesis mutants were created, PA23phaC, PA23phaC1ZC2 and PA23phaC1ZC2D, which no longer accumulated PHA. We observed that PA23phaC1ZC2D produced less PHZ compared to wild type (WT). All three mutants exhibited enhanced sensitivity to UV radiation, starvation, heat and cold stress, and exposure to hydrogen peroxide. Moreover, a lack of PHA production resulted in increased motility, biofilm formation, exopolysaccharide production and root attachment. Interaction studies with the protozoan predator II Ac revealed that the WT, PA23phaC1 and PA23phaC1ZC2 mutants were less palatable compared to the PA23phaC1ZC2D mutant, which produced less PHZ. Taken together, the accumulation of PHA enhances bacterial resistance to various stress conditions, which could improve the environmental fitness of this bacterium in hostile environments. III Acknowledgments First, I would like to express my deepest appreciation to my supervisor Dr. Teresa de Kievit for giving me the opportunity to work in her lab. Her supervision, support, intellectual guidance has inspired me throughout this journey and helped me to fulfill my lifetime desire to be a scientist. With her persistent help and advice, this thesis would not have been possible. I would also like to thank my committee members Drs. Ann Karen Brassinga, Silvia Cardona and Jillian Detwiler for their support, feedback and constructive suggestions they have given me over the last few years. I would like to thank Dr. Brassinga for allowing me to use her lab equipment and a special thanks to Dr. Jennifer Tanner for teaching me on how to work with A. castellanii. I would also like to extend my thanks to the wonderful past and present members of our lab: Munmun, Kelly, Sanjay, Nidhi, Amanda, Grace and April for their support and encouragement and for making the atmosphere full of joy. Finally, I would like to express my gratitude towards my family in Libya for their encouragement. My beloved and supportive wife, Ratiba who is always by my side when I needed her most and helped me a lot in making this journey, and my lovable children, Moyaed, Rawad and Larrain who served as my inspiration to complete this endeavor. IV Table of contents Abstract ............................................................................................................................................ II Acknowledgments ......................................................................................................................... IV Table of Contents ........................................................................................................................... V List of Tables ................................................................................................................................. IX List of Figures ................................................................................................................................. X List of Abbreviations ................................................................................................................... XII Chapter 1 ......................................................................................................................................... 1 1.1. Biological control of phytopathogens by Pseudomonas species ............................................ 2 1.1.1. Biological control .......................................................................................................... 2 1.1.2. Biocontrol activity of Pseudomonas species .................................................................... 3 1.2. Pseudomonas chlororaphis PA23 ......................................................................................... 4 1.3. P. chlororaphis PA23 biocontrol compounds ....................................................................... 4 1.3.1. Phenazines .................................................................................................................... 4 1.3.2. Pyrrolnitrin ................................................................................................................... 5 1.3.3. Hydrogen cyanide.......................................................................................................... 6 1.3.4. Siderophores ................................................................................................................. 7 1.3.5. Lytic enzymes ............................................................................................................... 8 1.4. Regulatory elements governing biocontrol activity in P. chlororaphis PA23 ........................ 8 1.4.1. Gac-Rsm signal transduction system ............................................................................. 10 1.4.2. Pseudomonas transcription regulator A ......................................................................... 12 1.4.3. Quorum sensing (QS) .................................................................................................. 12 1.4.4. RpoS and PsrA regulatory control ................................................................................. 14 1.4.5. ANR regulator ............................................................................................................. 15 1.5. Polyhydroxyalkanoates ..................................................................................................... 16 1.5.1. PHA biosynthesis pathways ......................................................................................... 17 1.5.2. The role of PHA in bacterial endurance against stress .................................................... 21 1.5.3. PHA in host-bacterial symbiosis ................................................................................... 21 1.6. Free-living amoebae .......................................................................................................... 22 1.6.1. Acanthamoeba castellanii ............................................................................................ 23 1.6.1.1. How intracellular bacteria survive in Ac ........................................................... 24 V 1.7. What makes a successful biocontrol agent? ....................................................................... 27 1.7.1. Bottom-up regulation ................................................................................................... 27 1.7.2. Top-down regulation ................................................................................................... 28 1.8. Bacterial defence against predators................................................................................... 29 1.8.1. Defence against predators: the effect of bacterial secondary metabolites .......................... 29 1.8.2. Morphological adaptation............................................................................................. 30 1.8.3. Biochemical surface properties ..................................................................................... 31 Chapter 2. Materials and Methods.............................................................................................. 33 2.1. Bacterial strains and growth conditions ............................................................................ 34 2.2. Acanthamoeba strain and culture conditions ..................................................................... 34 2.2.1. Reviving A. castellanii trophozoites from frozen stocks ................................................. 35 2.3. Nucleic acid manipulation ................................................................................................. 35 2.4. Generation of PA23phaC1, PA23phaC1ZC2, PA23phaC1ZC2D
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