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View of Investigations…………………………………………………...26 UNRAVELING GENETICALLY ENCODED PATHWAYS LEADING TO BIOACTIVE METABOLITES IN GROUP V CYANOBACTERIA by BRITTNEY MICHALLE BUNN Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy Dissertation Advisor: Dr. Rajesh Viswanathan Department of Chemistry CASE WESTERN RESERVE UNIVERSITY January, 2016 I CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of BRITTNEY MICHALLE BUNN candidate for the degree of Doctor of Philosophy*. Committee Chair Robert Salomon, PhD Committee Member Anthony Pearson, PhD Committee Member Michael Zagorski, PhD Committee Member John Mieyal, PhD Date of Defense August 31, 2015 *We also certify that written approval has been obtained for any proprietary material contained therein. II This thesis is dedicated to my parents, Glenn and Michalle Bunn. I am forever grateful for your boundless love and unwavering support and encouragement. III Table of contents Chapter 1: General Introduction…………………………………………………………..1 1.1 Introduction to Cyanobacteria…………………………………………………2 1.2 Cyanobacteria as a Source of Bioactive Natural Products……………………...3 1.3 Cyanobacterial Natural Product Biosyntheses…………………………….…...6 1.4 Group V Cyanobacteria’s Hapalindole-type Alkaloid Family of Natural Products…………………………………………………………………..10 1.5 Hapalindole-type Alkaloid Biosynthesis……………………………….…….19 1.6 Synthetic Biology Approach to Bioactive Natural Products……………….…23 1.6.1 Introduction to Synthetic Biology as a Tool for Biosynthetic Investigations…………………………………………………….23 1.6.2 Introduction to Synthetic Biology as a “Green” Synthesis Methodology Toward Novel Natural Product Analogs…………..25 1.7 Overview of Investigations…………………………………………………...26 1.7.1 Heterologous Expression and in vitro Reconstitution of Isonitrile Synthase (WelI1) and Fe(II)-α-Ketoglutarate Dependent Oxygenase (WelI3)…………………………………………………………...26 1.7.2 Substrate Tolerance of Isonitrile Synthase and Fe(II)-α-Ketoglutarate Dependent Dioxygenase affords Unnatural Variants of Cyanobacterial Hapalindole Pathway Intermediate………………27 1.8 References…………………………………………………………………....28 IV Chapter 2: Heterologous Expression and in vitro Reconstitution of Isonitrile Synthase (WelI1) and Fe(II)-α-Ketoglutarate Dependent Oxygenase (WelI3)………………….…41 2.1 Introduction……………………………………….………………………….42 2.2 Results and Discussion………………………….……………………………44 2.2.1 Identification of the Putative Hapalindole-type Alkaloid Biosynthetic Gene Cluster……………………………………………………...44 2.2.2 Bioinformatic Analysis of WelI1/3 & Homology to IsnA/B and PvcA/B…………………………………………………………...45 2.2.3 In vitro Reconstitution and Unambiguous Characterization of WelI1 and WelI3………………………………………………………...52 2.3 Conclusion……………………………………….…………………………...58 2.4 Experimental Section………………………………………………………...61 2.4.1 Cyanobacterial Culturing…………………………………………..61 2.4.2 Genomic DNA Extraction………………………………………….61 2.4.3 Whole Genome Sequencing and Bioinformatics………….……….62 2.4.3.1 Homology Based Model Generation……………………..63 2.4.3.2 Nucleotide Accession Numbers…………………………..63 2.4.4 Gene Cloning for Heterologous Expression……………………......63 2.4.5 Heterologous Expression of WelI1 and WelI3……………………..63 2.4.6 Enzymatic Assay with Cell Lysates Containing WelI1 and WelI3 for GC-MS and LC-MS……………………………………………...64 2.4.7 GC-MS Analysis…………………………………………….…..…65 2.4.8 LC-MS Analysis……………………………………………………65 V 2.4.9 Enzymatic Assay with Cell Lysates Containing WelI1 and WelI3 for HPLC…………………………………………………………….66 2.4.10 HPLC Analyses……………..……………………….…….……...66 2.4.11 Synthesis and Spectroscopic Analysis of Indole-isonitrile…….…67 2.4.11.1 Synthesis of Cis and Trans Isomers of Indole- isonitrile………………………………………….68 2.4.11.1.1 Synthesis of 3-Indolecarbaldehyde (Precursor for Indole-isonitrile Synthesis………………………..68 2.4.11.1.2 Synthesis of Indole-isonitrile (3-(2- Isocyanovinyl)indole)……………………………68 2.4.11.2 Spectroscopic Analysis of Indole-isonitrile…………….69 2.4.11.2.1 Cis Indole-isonitrile 1H and 13C NMR Data......68 2.4.11.2.2 Trans Indole-isonitrile 1H and 13C NMR Data...69 2.5 References…………….……………………………………………………...70 VI Chapter 3: Substrate Tolerance of Isonitrile Synthase and Fe(II)-α-Ketoglutarate Dependent Dioxygenase affords Unnatural Variants of Cyanobacterial Hapalindole Pathway Intermediate…………………………………………………………………….73 3.1 Introduction…………………………….…………………………………….74 3.1.1 Assessing the Substrate Promiscuity of WelI1 and WelI3………….74 3.1.2 Tri-Catalytic Biosynthetic Methodology to Access Novel Natural Product Analogs………………………………………………….77 3.2 Results and Discussion………………………………………………………78 3.2.1 Heterologous Expression and Purification of WelI1 and WelI3……78 3.2.2 Heterologous Expression, Purification, and Enzymatic Assay of TmTrpB1…………………………………………………………79 3.2.3 Assessment of Substrate Promiscuity of WelI1 and WelI3………...81 3.2.4 Homology-based Model Building and in silico Docking……….…85 3.3 Conclusion……………………………………………………………......….90 3.4 Experimental Section………………………………………………………...91 3.4.1 WelI1 and WelI3…………………………………………………...91 3.4.1.1 Vector Selection…………………………………….……91 3.4.1.2 Transformation…………………………………….……..91 3.4.1.3 Culturing and Induction……………………………….….91 3.4.1.4 Lysis………………………………………………….…..92 3.4.1.5 Purification……………………………………………….92 3.4.2 Enzymatic Assay with Purified WelI1 and WelI3……………….….93 3.4.2.1 General Procedure………………………………….…….93 VII 3.4.2.2 HPLC Analysis of Enzymatic Assay Extracts……………94 3.4.2.3 LC-HRMSMS Analysis………………………………….95 3.4.3 TmTrpB1…………………………………………………….……..96 3.4.3.1 Culturing and Induction………………………………….96 3.4.3.2 Lysis……………………………………….……………..96 3.4.3.3 Purification…………………………………….…………97 3.4.3.4 Enzymatic Assay with Purified TmTrpB1……….……….97 3.5 References………………………………………………….………………...99 VIII Chapter 4: Thesis Summary and Future Directions……………………………………..102 4.1 Thesis Summary……………………………………………………….……102 4.1.1 Part I: Heterologous Expression and in vitro Reconstitution of Isonitrile Synthase (WelI1) and Fe(II)-α-Ketoglutarate Dependent Oxygenase (WelI3)………………………………...…………...102 4.1.2 Part II: Substrate Tolerance of Isonitrile Synthase and Fe(II)-α- Ketoglutarate Dependent Dioxygenase Affords Unnatural Variants of Cyanobacterial Hapalindole Pathway Intermediate……….…104 4.2 Future Directions………………………………………….………………...106 4.3 References……………………….………………………………………….108 Appendix 1 Bioinformatic Analysis of WelI1 and WelI3……………………………….111 Appendix 1.1 Illustration of Gene Clusters…….……….……………………...111 Appendix 1.2 Translation of welI1 and welI3 using ExPaSy’s Translate Tool.....112 Appendix 1.2.1 Translation of welI1……………………………….…...112 Appendix 1.2.2 Translation of welI3…………………………….……...112 Appendix 1.3 BLASTP Results for WelI1 and WelI3……….………………....113 Appendix 2 Cis and Trans Indole-Isonitrile Synthetic Standard Characterization……..115 Appendix 2.1 NMR Spectra……………………………………………………115 Appendix 2.2 HRMS Spectra………………………………………….………..117 Appendix 3 Analysis of WelI1/3 Enzymatic Assays with E. coli Cell Lysates….…...…118 Appendix 3.1 Analysis of WelI1/3 Enzymatic Assay by LC-MS……………....118 Appendix 4 GC-MS Spectra of Synthesized Cis and Trans Indole-Isonitrile Standards119 Appendix 5 NMR Spectra of 2-Methyl-L-Tryptophan………………..………………...123 IX Appendix 6 Analysis of WelI1/3 Enzymatic Assay Results with L-Tryptophan and Tryptophan Analogs……………..……………………………………………...125 Appendix 6.1 HPLC Analysis…………………………………………………..125 Appendix 6.2 LC-MS and MSMS Analysis of WelI1/3 Enzymatic Assay Results with L-Tryptophan and Tryptophan Analogs…………………………...126 Appendix 6.2.1 Assay with L-Tryptophan…………………………..…….……126 Appendix 6.2.2 Assay with 2-Methyl-L-Tryptophan…………………..…………….…128 Appendix 6.2.3 Assay with 1-Methyl-L-Tryptophan……………………..…….………130 Appendix 6.2.4 Assay with 4-Fluoro-DL-Tryptophan……………………..…………...132 Appendix 6.2.5 Assay with 5-Methyl-DL-Tryptophan……...………………………….134 Appendix 6.2.6 Assay with 6-Methyl-DL-Tryptophan……………………….…..…….136 Appendix 6.2.7 Assay with 5-Methoxy-L-Tryptophan……………………...………….138 Appendix 6.2.8 Assay with 5-Hydroxy-L-Tryptophan………………………….……...140 Appendix 7 WelI3 Homology Modeling, Docking and Multiple Alignments…………..142 Appendix 7.1 Method for Generation of Homology Model for WelI3………………....142 Appendix 8 References to Appendices………………………………………………….143 Bibliography……………………………………………………………………………144 X List of Tables Table 1.1 Hapalindole analogs that have been isolated from group V cyanobacteria…...11 Table 1.2 Fischerindole analogs isolated from group V cyanobacteria………………….14 Table 1.3 Ambiguine analogs isolated from group V cyanobacteria……………………15 Table 1.4 Welwitindolinone analogs isolated from group V cyanobacteria…………….17 Table 3.1 List of LC-MS retention times, molecular formulas, percent yields, and MS2 fragmentation patterns for products (3.3a-h)……………………………………..84 Table 3.2 Total volume, protein volume, and protein concentration data for assays with purified WelI1 and WelI3………………………………………………………..93 Table A1.1 BLASTP results for WelI1………………………………………………...113 Table A1.2 BLASTP results for WelI3………………………………………………...114 XI List of Figures Figure 1.1 Chemical structures of well-known cyanobacterial toxic natural products…...4 Figure 1.2 Chemical structures of cyanobacterial natural products with therapeutic potential due to their interesting bioactivities. Hapalosin (1.4) has shown anti- MDR properties and dolastatin 10 (1.5) has shown to be cytotoxic………..……...6 Figure 1.3 Graphical representation of available cyanobacterial genomes……………….9 Figure 1.4 Structures of the first isolated hapalindole-type alkaloids, hapalindole A (1.6) and hapalindole B
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