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The Evolutionary Diversity and Biological Function of Phenazine Metabolite Biosynthesis in Burkholderia SPP

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The Evolutionary Diversity and Biological Function of Phenazine Metabolite Biosynthesis in Burkholderia SPP The University of Southern Mississippi The Aquila Digital Community Master's Theses Summer 2019 The Evolutionary Diversity and Biological Function of Phenazine Metabolite Biosynthesis in Burkholderia SPP Samuel Hendry University of Southern Mississippi Follow this and additional works at: https://aquila.usm.edu/masters_theses Part of the Bacteriology Commons Recommended Citation Hendry, Samuel, "The Evolutionary Diversity and Biological Function of Phenazine Metabolite Biosynthesis in Burkholderia SPP" (2019). Master's Theses. 653. https://aquila.usm.edu/masters_theses/653 This Masters Thesis is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Master's Theses by an authorized administrator of The Aquila Digital Community. For more information, please contact [email protected]. THE EVOLUTIONARY DIVERSITY AND BIOLOGICAL FUNCTION OF PHENAZINE METABOLITE BIOSYNTHESIS IN BURKHOLDERIA SPP by Samuel Hendry A Thesis Submitted to the Graduate School, the College of Arts and Sciences and the School of Biological, Environmental, and Earth Sciences at The University of Southern Mississippi in Partial Fulfillment of the Requirements for the Degree of Master of Science Approved by: Dmitri Mavrodi, Committee Chair Janet Donaldson Mohamed Elasri ____________________ ____________________ ____________________ Dr. Dmitri Mavrodi Dr. Jake Schaefer Dr. Karen S. Coats Committee Chair Director of School Dean of the Graduate School August 2019 COPYRIGHT BY Samuel Hendry 2019 Published by the Graduate School ABSTRACT Burkholderia encompass a group of ubiquitous Gram-negative bacteria that include numerous saprophytes, as well as several species that cause infections in animals, immunocompromised patients, and plants. Some species of Burkholderia produce colored redox-active secondary metabolites called phenazines (Phz). In the model opportunistic pathogen Pseudomonas aeruginosa, phenazines strongly contribute to the competitiveness, formation of biofilms, and virulence in multiple models of infection. Similar depth of knowledge on the diversity, biosynthesis, and biological functions of phenazines in Burkholderia is missing. This project aimed to bridge this gap in knowledge by focusing on phenazine pathways of B. lata and closely related species. My results revealed that phz genes are present in genomes of many Burkholderia that have a worldwide origin and belong to different species of the genus. Most Phz+ strains were in the Bcc group, but the capacity to synthesize phenazines was also found in some isolates of the B. pseudomallei clade and the plant pathogen B. glumae. My findings also suggest that the phenazine biosynthetic pathway of Burkholderia has a complex evolutionary history, which likely involved horizontal gene transfers among several distantly related groups of producing organisms. I also analyzed isogenic mutants and plasmid deletion derivatives of Burkholderia lata, which helped to identify phenazines produced by species of the ubiquitous B. cepacia (Bcc) group and characterize the role of phenazine- modifying genes in the synthesis of 4,9-dihydroxyphenazine-1,6-dicarboxylic acid dimethylester. My functional studies failed to link the production of phenazines with the capacity of Burkholderia to kill fruit flies and rot onions, but other experiments revealed ii a link between the presence and amount of phenazines and the dynamics of biofilm growth flow in the flow cell and static experimental systems. iii ACKNOWLEDGMENTS I would like to express my deepest gratitude to Drs. Dmitri Mavrodi and Olga Mavrodi. Without heir tireless work, motivation, and never-ending help, I would have never reached this point in my education. The high standards implemented in their lab allowed for me to grow into a confident and well-rounded researcher. Thanks to my committee member Dr. Mohamed Elasri for teaching me and sharing his equipment and wealth of knowledge in the realm of biofilm studies. Thanks also to my committee member Dr. Janet Donaldson for her help and encouragement, as well as teaching me much in bacteriology. I also thank Dr. Wulf Blankenfeldt and Stephan Steinke from the Helmholtz Center for Infection Research in Germany for their assistance in extracting and performing analytical analyses on phenazine metabolites. I could not have done this without my supportive and loving wife, Mary Katherine, and our dog Luna. Many thanks to my Mavrodi lab family for all their help. This work was supported by startup funds in Dr. Mavrodi’s lab, the EAGLE Scholarship Program for Undergraduate Research, and by Mississippi INBRE, funded by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under grant number P20GM103476. iv TABLE OF CONTENTS ABSTRACT ........................................................................................................................ ii ACKNOWLEDGMENTS ................................................................................................. iv LIST OF TABLES ............................................................................................................ vii LIST OF ILLUSTRATIONS ........................................................................................... viii LIST OF ABBREVIATIONS ............................................................................................ ix CHAPTER I – INTRODUCTION ...................................................................................... 1 1.1 Burkholderia spp. are diverse and economically important microorganisms........... 1 1.2 The diversity and biosynthesis of microbial phenazines .......................................... 5 1.3 Biological function of phenazine metabolites........................................................... 8 1.4 Phenazine production in Burkholderia spp. ............................................................ 11 1.5 Aims of this study ................................................................................................... 12 CHAPTER II - MATERIALS AND METHODS ............................................................ 14 2.1 Screening the newly-sequenced and publicly-available genome sequences of Burkholderia for the presence of phenazine biosynthesis genes. ................................. 14 2.2 Genetic analysis of phenazine biosynthesis in Burkholderia spp. .......................... 16 2.3 Pathogenicity assays with the fruit fly Drosophila melanogaster and onions ........ 17 2.4 Flow cell and static biofilm assays ......................................................................... 18 CHAPTER III – RESULTS .............................................................................................. 21 3.1 Screening Burkholderia genomes for the presence of phenazine genes ................. 21 v 3.2 Genetic analysis of phenazine biosynthesis in B. lata ATCC 17760 ..................... 27 3.3 Biological function of phenazine compounds in B. lata ATCC 17760 .................. 30 CHAPTER IV – DISCUSSION........................................................................................ 38 REFERENCES ................................................................................................................. 43 vi LIST OF TABLES Table 3.1. Dose-response assays with B. cepacia ATCC 25416 and B. lata ATCC 17760 ........................................................................................................................................... 32 Table 3.2. Fruit fly pathogenicity assays with B. lata ATCC 17760 and its isogenic phenazine mutant derivatives ............................................................................................ 33 Table 3.3. Onion tissue maceration assays with different Burkholderia spp .................... 34 vii LIST OF ILLUSTRATIONS Figure 1.1 Phenazine metabolites and biosynthesis ............................................................ 7 Figure 3.1 16s rRNA phylogeny of Burkholderia spp. ..................................................... 22 Figure 3.2 Multi-locus sequence typing phylogeny of Burkholderia spp. ....................... 23 Figure 3.3 Contrasting phylogenies using phz proteins and housekeeping enzymes ....... 24 Figure 3.4 Gene organization of various Burkholderia phz loci ...................................... 25 Figure 3.5 Flanking regions surrounding the phz loci ...................................................... 27 Figure 3.6 Phenazine intermediates identified from culture of B. lata ATCC 17760 ...... 29 Figure 3.7 Genetic organization of phz gene cluster in B. lata ATCC 17760 .................. 30 Figure 3.8 Survival curves for D. melanogaster infected with Burkholderia spp. ........... 31 Figure 3.9 Onion tissue maceration by B. cepacia ATCC 25416 ..................................... 34 Figure 3.10 Graph of % coverage of biofilm in BioFlux microfluidistic system ............. 36 Figure 3.11 Static biofilm formation ................................................................................ 37 viii LIST OF ABBREVIATIONS AOCHC 6-amino-5-oxocyclohex-2-ene-1-carboxylic acid Bcc Burkholderia cepacia complex DHHA trans-2,3-dihydro-3-hydroxyanthranilic acid KMB King’s Medium B Broth PCA Phenazine-1-carboxylic acid PDC Phenazine-1,6-dicarboxylic acid Phz Phenazine TSB Tryptic Soy Broth ix CHAPTER I – INTRODUCTION 1.1 Burkholderia spp. are diverse and economically important microorganisms Burkholderia is a ubiquitous group of Gram-negative bacteria that
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