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Download The SIDEROPHORE-MEDIATED IRON METABOLISM IN STAPHYLOCOCCUS AUREUS by Marek John Kobylarz B.Sc., The University of Victoria, 2010 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Microbiology and Immunology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) February 2016 © Marek John Kobylarz, 2016 Abstract Staphylococcus aureus requires iron as a nutrient and uses uptake systems to extract iron from the human host. S. aureus produces the iron-chelating siderophore staphyloferrin B (SB) to scavenge for available iron under conditions of low iron stress. Upon iron-siderophore re-entry into the cell, iron is separated from the siderophore complex to initiate assimilation into metabolism. To gain insight into how SB biosynthesis is integrated into S. aureus central metabolism, the three SB precursor biosynthetic proteins, SbnA, SbnB, and SbnG, were biochemically characterized. SbnG is a citrate synthase analogous to the citrate synthase enzyme present in the TCA cycle. The crystal structure of SbnG was solved and superpositions with TCA cycle citrate synthases support a model for convergent evolution in the active site architecture and a conserved catalytic mechanism. Since L-Dap is an essential precursor for SB, the biosynthetic pathway for L-Dap was elucidated. A combination of X-ray crystallography, biochemical assays and biophysical techniques were used to delineate the reaction mechanisms for SbnA and SbnB, demonstrating that SbnA performs a -replacement reaction using O-phospho-L-serine (OPS) and L-glutamate to produce N-(1-amino-1-carboxy-2-ethyl)-glutamic acid (ACEGA). Oxidative hydrolysis of ACEGA catalyzed by SbnB produces -ketoglutarate and L-Dap. Detailed analysis of the substrate specificity of SbnA revealed that OPS binding and conversion to the PLP-- aminoacrylate intermediate in SbnA induced a conformational change and formation of a second substrate binding pocket for L-glutamate. Furthermore, L-cysteine was identified as a competitive inhibitor of SbnA activity, revealing a link between iron uptake and the oxidative stress response in S. aureus. IruO was examined for its role in Fe(III)-siderophore reduction. ii Utilizing a combination of visible spectroscopy and enzyme kinetics, a mechanism for electron transfer was proposed. IruO was demonstrated to reduce iron bound hydroxamate-type siderophores to release Fe(II) using NADPH as the electron donor. Under anaerobic conditions, IruO formed a stable FAD semiquinone intermediate that mediates a single electron transfer from the FAD to the Fe(III)-siderophore complex. These studies have shown how SB precursors are synthesized and led to the development of models for SB biosynthesis integration into central metabolism under conditions of low iron stress. iii Preface Most of the work presented in this thesis is published or drawn from manuscripts under preparation. The following contributions were made by fellow scientists and collaborators: Chapter 3 Kobylarz, M.J., Grigg, J.C., Sheldon, J.R., Heinrichs, D.E., and Murphy, M.E.P. (2014) SbnG, a citrate synthase in Staphylococcus aureus: a new fold on an old enzyme, J. Biol. Chem. 289, 33797-33807. Chapter 3 was derived from the published manuscript. Dr. D.E. Heinrichs provided the sbnG plasmid construct. Dr. J.C. Grigg developed the protein expression and purification protocols. I optimized crystallization conditions, determined the structure of SbnG and performed bioinformatics analyses. J.R. Sheldon generated SbnG variant complementation vectors (Tables 2-1 and 2-2) and analyzed SbnG activity in S. aureus, which is presented in Figure 3-5. I wrote the first draft of the manuscript with contributions from J.R. Sheldon on the methods and results. The manuscript was edited by Dr. J.C. Grigg, Dr. D.E. Heinrichs, and Dr. M.E.P. Murphy. Chapter 4 Kobylarz, M.J., Grigg, J.C., Takayama, S.J., Rai, D.K., Heinrichs, D.E., and Murphy, M.E.P. (2014) Synthesis of L-2,3-diaminopropionic acid, a siderophore and antibiotic precursor, Chem. Biol. 21, 379-388. iv Chapter 4 was assembled from the published manuscript. Dr. D.E. Heinrichs provided the sbnA and sbnB plasmid constructs. Dr. J.C. Grigg and D.K. Rai were responsible for solving the structure of SbnB in both the apo- and NAD+ bound form, which are presented in Figure 4-9. Dr. S.J. Takayama performed the NMR small molecule analysis of ACEGA and the results are presented in Figure 4-3 and Table 4-1. I optimized the protein expression and purification for SbnA and SbnB, performed all activity assays and visible spectroscopic analysis. I also solved the structure of SbnB with bound ligands ACEGA and NAD+, and -KG and NADH. I wrote the first draft of the manuscript. Dr. S.J. Takayama provided the NMR results and figures. The manuscript was edited by Dr. J.C. Grigg, Dr. D.E. Heinrichs, and Dr. M.E.P. Murphy. Chapter 5 Kobylarz, M.J., Grigg, J.C., Liu, Y., Lee, M.S.F., Heinrichs, D.E., and Murphy, M.E.P. (2015) Deciphering the substrate specificity of SbnA, the enzyme catalyzing the first step in staphyloferrin B biosynthesis. Accepted by Biochemistry. Chapter 5 was derived from the manuscript currently submitted and under review. Dr. J.C. Grigg and M.S.F. Lee solved the wild type structure of SbnA, which is presented in Figure 5-1. I optimized the purification protocol for SbnA, identified new SbnA crystallization conditions, solved the structure of SbnA bound to its substrate O-phospho-L-serine and designed all kinetic analysis assays. Y. Liu generated the SbnA active site variants and performed both steady-state kinetic and single turnover analysis on the SbnA variants and the results are presented in Figures 5-5, 5-6, 5-9, 5-13 and 5-14 and Tables 5-1, 5-2 and 5-3. Y. Liu also crystallized and solved the structures of SbnA Y152F and SbnA Y152F/S185G (Figure 5-11). I v wrote the first draft of the manuscript while J.C. Grigg, Dr. D.E. Heinrichs and Dr. M.E.P. Murphy edited the manuscript. Chapter 6 Kobylarz, M.J., Heieis, G.A., Loutet, S.A., and Murphy, M.E.P. (2015) The siderophore reductase IruO uses an FAD semiquinone intermediate to catalyze iron reduction. Manuscript in preparation. Chapter 6 is a draft of a manuscript that will be submitted. I did the cloning, protein expression and purification, and structure determination of IruO. I also measured the sulfhydryl content of IruO, performed the visible spectroscopic analysis of IruO and developed all kinetic analysis assays. G.A. Heieis performed all the kinetic analysis assays, fluorescence spectroscopy and anaerobic visible absorption spectroscopy, which is presented in Figures 6-8, 6-9, 6-11 and 6-12 and Table 6-1. Dr. S.A. Loutet purified IsdI, did the heme degradation assays (Figure 6-10) and wrote the corresponding methods and results sections. I wrote the first draft of the manuscript. Biosafety Approval This project required Biohazard Approval for the handling of Staphylococcus aureus and Escherichia coli and was issued by the UBC Biosafety Committee, Certificate number B13- 0096. vi Table of Contents Abstract .......................................................................................................................................... ii Preface ........................................................................................................................................... iv Table of Contents ........................................................................................................................ vii List of Tables .............................................................................................................................. xiii List of Figures ............................................................................................................................. xiv List of Abbreviations ............................................................................................................... xviii Acknowledgements ................................................................................................................... xxii Chapter 1: Introduction ................................................................................................................1 1.1 Staphylococcus aureus .................................................................................................... 1 1.2 Staphylococcus aureus iron uptake systems ................................................................... 3 1.2.1 Heme uptake ............................................................................................................... 4 1.2.2 Siderophore uptake systems ........................................................................................ 4 1.2.2.1 Hydroxamate-type siderophore uptake ............................................................... 9 1.2.2.2 Catecholate-type siderophore uptake ................................................................ 11 1.2.2.3 Staphyloferrin (SA) and (SB) uptake ................................................................ 12 1.3 Siderophore biosynthesis in Staphylococcus aureus .................................................... 13 1.3.1 Staphyloferrin A........................................................................................................ 14 1.3.2 Staphyloferrin B ........................................................................................................ 14 1.4 Iron uptake systems in other Staphylococcus species ..................................................
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