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BIOSYNTHESIS of PRODIGININE and TAMBJAMINE NATURAL PRODUCTS in PSEUDOALTEROMONAS SP. by Katherine J. Picott a Thesis Submitted T

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BIOSYNTHESIS OF PRODIGININE AND TAMBJAMINE NATURAL PRODUCTS IN PSEUDOALTEROMONAS SP. by Katherine J. Picott A thesis submitted to the Department of Biomedical and Molecular Sciences in conformity with the requirements for the degree of Master of Science Queen’s University Kingston, Ontario, Canada October, 2018 Copyright © Katherine J. Picott, 2018 ‘The more that you read, the more things you will know. The more that you learn, the more places you’ll go” – Dr. Suess ii Abstract Prodiginines and tambjamines are two classes of pigmented natural products that display structural variety and hold many useful bioactivities, making them a desirable target for pharmaceutical agents1. Enzymes PigC and TamQ are responsible for the final step in prodiginine and tambjamine biosynthesis respectively, involving the coupling of a product specific intermediate to the shared intermediate 4-methoxy-2,2’-bipyrrole-5-carbaldehyde2. Previous investigations have focused solely on PigC and have not successfully purified the enzyme, inciting the use of crude cell lysate to test enzyme activity3,4. The objectives of this research were to directly compare the kinetic characteristics and substrate selectivity of PigC and TamQ. PigC was cloned from Pseudoalteromonas rubra, a known producer of several prodiginine analogues5,6. TamQ was cloned from Pseudoalteromonas citrea, which is predicted to produce tambjamine YP1 based on genomic mining. PigC and TamQ were successfully heterologously expressed and purified, and enzymatic activities of both PigC and TamQ were reconstituted with their native and pseudo-native substrates. The true kinetic parameters of two substrates for PigC were determined, allowing for prediction of the reaction sequence and a proposed Ter Bi Ping Pong enzyme system. PigC also demonstrated some substrate flexibility by accepting a synthetic halogenated analogue in addition to its natural substrate 2-methyl-3-amyl-pyrrole (MAP). Apparent kinetic values for TamQ were obtained using a close analogue of its native substrate. Additionally, the enzyme could accept and turnover the PigC substrate MAP, though, the structure of the reaction product has yet to be determined. Three other biosynthetic enzymes involved in tambjamine YP1 (TamA, TamT, and TamH) construction were cloned from P. citrea and expressed for future functionality studies. Lastly, a novel cyclized variant of tambjamine YP1 was isolated from P. citrea. The complete structure of this compound was determined by NMR and X-ray crystallography analysis. iii Co-Authorship Katherine Picott initiated this project and was involved all experimental development. Research presented in this thesis was performed by Katherine Picott and Ella Dekemp. Julie Deichert synthesized and provided all monopyrrole compounds used as substrates for PigC and TamQ. Françoise Sauriol acquired all NMR data measured on the Bruker AVANCE-600 MHz and NEO 700 MHz instruments. Gabriele Schatte collected all X-ray crystallographic data, solved, and refined the crystal structure of the cyclic tambjamine YP1 analogue. Under the supervision of Katherine Picott, Ella Dekemp constructed the expression vectors for TamA and TamH, purified TamH, and assisted with kinetic measurements of PigC and TamQ. iv Acknowledgments First, I would like to thank my supervisor Zongchao Jia, for guiding me through this degree and providing new insight on my research. To my committee member David Zechel, thank you for everything you taught me and your enthusiasm throughout the years. Thank you to Julie, without all of your hard work this thesis would be half as long, I am excited for you to continue this project, I cannot wait to see where it goes. Ella, thank you for all of your effort in the lab, for all your difficult questions that forced me to really think, and for your friendship the past year and a half. Thank you to the rest of the Ross Lab for helping me enjoy being in the lab every day. It was a pleasure to be your lab mom, I will miss working with each of you. Thank you to Shalandra, for being an incredible friend and editor. To Mitchell, thank you for keeping me sane and for pretending you know what I am talking about when I tell you about my results. Finally, thank you to my supervisor Avena Ross, for all that you have done for me these past few years. Your mentorship and support, both inside and outside of the lab, have meant the world to me. You have introduced me to a field of research that I love and given me the opportunity to grow as a scientist. Thank you for everything. v Statement of Originality I hereby state that the contents of this thesis are the author’s original work. Any ideas, techniques, and/or data from the work of others, published or unpublished, are recognized and fully attributed to the original source in agreement with standard referencing conventions. (Katherine J. Picott) (October, 2018) vi Table of Contents Abstract .......................................................................................................................................... iii Co-Authorship................................................................................................................................ iv Acknowledgments ........................................................................................................................... v Statement of Originality ................................................................................................................. vi Table of Contents .......................................................................................................................... vii List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................. x List of Abbreviations ................................................................................................................... xiii Introduction ............................................................................................................... 1 Literature Review ..................................................................................................... 4 2.1 Pseudoalteromonas sp. ........................................................................................................................4 2.2 Prodiginines .........................................................................................................................................5 2.3 Tambjamines .......................................................................................................................................8 2.4 Prodiginine and Tambjamine Structural Features ...............................................................................9 2.5 Prodiginine and Tambjamine Bioactivities .......................................................................................11 2.6 Prodiginine and Tambjamine Biosynthesis .......................................................................................13 2.6.1 General Biosynthetic Scheme of Prodiginines and Tambjamines .............................................13 2.6.2 Identification of the red, pig, and tam Clusters ..........................................................................14 2.6.3 MBC Identification and Biosynthesis ........................................................................................16 2.6.4 pig and red Pathways .................................................................................................................19 2.6.5 tam Pathway ...............................................................................................................................21 2.6.6 Condensation Reaction ...............................................................................................................23 2.7 Condensation Enzyme Characterization ............................................................................................23 2.7.1 Homologous Protein Domains ...................................................................................................23 2.7.2 Predicted Enzymatic Mechanism ...............................................................................................24 2.7.3 Substrate Selection .....................................................................................................................26 2.8 Thesis Objectives ...............................................................................................................................27 Experimental ........................................................................................................... 28 3.1 Materials ............................................................................................................................................28 3.2 Equipment ..........................................................................................................................................31 3.2.1 HPLC-PDA and UPLC-PDA-MS Purification and Analysis ....................................................31 3.2.2 High-Resolution Mass Spectrometry .........................................................................................31 3.2.3 NMR Spectroscopy ....................................................................................................................32 3.2.4 X-Ray Crystallography ..............................................................................................................32
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