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UNIVERSITY of CALIFORNIA, SAN DIEGO Novel Biodiversity of Natural UNIVERSITY OF CALIFORNIA, SAN DIEGO Novel Biodiversity of Natural Products-producing Tropical Marine Cyanobacteria A Dissertation submitted in partial satisfaction of the requirement for the degree Doctor of Philosophy in Oceanography by Niclas Engene Committee in Charge: Professor William H. Gerwick, Chair Professor James W. Golden Professor Paul R. Jensen Professor Brian Palenik Professor Gregory W. Rouse Professor Jennifer E. Smith 2011 UMI Number: 3473612 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent on the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. UMI 3473612 Copyright 2011 by ProQuest LLC. All rights reserved. This edition of the work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, MI 48106 - 1346 Copyright Niclas Engene, 2011 All rights reserved. The Dissertation of Niclas Engene is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2011 iii DEDICATION This dissertation is dedicated to everyone that has been there when I have needed them the most. iv TABLE OF CONTENTS Signature Page …………………………………………………..……………………... iii Dedication ……………...………………………………………………………..….….. iv Table of Contents ………...…………………………………………………..…………. v List of Figures ……………………………………………………………………..…… ix List of Tables …………………………………………………………..…………..….. xii List of Abbreviations ………......……………………………………..………….…… xiv Acknowledgments ...…………………………………….……………………..…..… xvii Vita …………………………………………………………………………..……........ xx Abstract …………………………………………………………………………..….. xxiv Chapter I.Introduction ……………………..……………………………………..……… 1 Natural Products as Ancient Medicine ……….….…………………….…….……. 2 Marine Natural Products …………………….….………………….……….…….. 3 Cyanobacterial Natural Products …………………….….………………….……. 10 Current Perspective of the Taxonomic Distribution of Natural Products in Marine Cyanobacteria ………………………….….…………………………….…….…. 11 Phylogenetics to Comprehend and Uncover Cyanobacterial Biodiversity ……..… 16 Rationale for Thesis Research …………….….……………………….…..……… 17 Overview of Thesis Chapters …………….….……………………….……..…….. 18 References …………………………………….….…………………..……….…... 22 v Chapter II. Phylogeny-guided Isolation of Ethyl Tumonoate A from the Marine Cyanobacterium cf. Oscillatoria margaritifera .………..………..………….......... 26 Abstract ………………………………………………………………..………..… 27 Introduction …………………………………….……………………..………....... 28 Materials and Methods …….…………………………………………..………….. 30 Results and Discussion ……………………………..………………..…………… 38 Conclusions ………..………………………………………………..………..…… 52 Acknowledgments ……………………………………………...…………..……... 54 Appendix ………………………………………….…………………………….… 55 References ……………………………………………………….……..…………. 64 Chapter III. 16S rRNA Gene Heterogeneity in the Filamentous Marine Cyanobacterial Genus Lyngbya ……………………………………………………….....………… 68 Abstract ……………………………………………………………..…………..… 69 Introduction …………………………………….………………………..………... 71 Materials and Methods …….……………………………………………..……….. 74 Results ………………………………………………………………..…………… 80 Discussion …………………………………………………………..…………….. 98 Acknowledgments …………………………………………………...………..…. 104 Appendix ……………………………….………….…………..…….....………... 105 References ……………………………………………………………..………… 111 vi Chapter IV. Intra-genomic 16S rRNA Gene Heterogeneity in Cyanobacterial Genomes ………………………….……................................................................................ 113 Abstract ……………………………………………………….………………… 114 Introduction …………………………………….……………….……………..... 115 Materials and Methods …….……………………………………..……………… 116 Results and Discussion ……………………………..…………………………… 117 Conclusions ………..…………………………………..……………………..….. 132 Acknowledgments …………………………………..………….…………..……. 133 References …………………………………………………………...…………... 134 Chapter V. Underestimated Biodiversity as a Major Explanation for the Perceived Rich Secondary Metabolite Capacity of the Cyanobacterial Genus Lyngbya………… 136 Abstract ……………………………………………………………..…………… 137 Introduction ………………………………………….…………..………………. 138 Materials and Methods …….………………………………………..…………… 141 Results ……………………………………………………………..…………….. 148 Discussion ……………………………………………………..………..……….. 167 Acknowledgments …………………………………….……………..…………... 172 References …………………………………………….……………..…………... 173 Chapter VI. Moorea gen. nov. (Cyanobacteria), a Tropical Marine Cyanobacterial Genus Rich in Bioactive Secondary Metabolites ……………………………………..… 177 Abstract ………………...……..………………………..………………………... 178 vii Introduction …………………...……………….………………………………… 179 Materials and Methods …….…………………………..………………………… 180 Results and Discussion ………..…………………………..……………..……… 184 Acknowledgments …………………...…...…………......………..……………… 201 Appendix ………………………………………….……………....……………... 202 References ………………………....……………….…………..………………... 209 Chapter VII. Taxonomic Distribution of Marine Cyanobacterial Natural Products …...………..………………………………………................................................ 212 Abstract ………………...……..……………………………………..…………... 213 Introduction …………………...………………………………………..………... 214 Materials and Methods …….………………………………………..…………… 216 Results and Discussion ………..……………………………………..……..…… 218 Conclusions ………..…………………………………..……………………..….. 237 Acknowledgments …………………...…...…………......…………..…………… 239 Appendix ………………………………………….…………..……………..…... 243 References ………………………....……………….………………………......... 243 Chapter VIII. Conclusion ………………………...………………...………..……… 253 viii LIST OF FIGURES Figure I.1: Ancient natural products .…………………..………...................................... 2 Figure I.2: Marine natural products .…………………..………....................................... 5 Figure I.3: Current perception of taxonomic distribution of natural products in marine cyanobacteria .……………………………………………………………..…… 14 Figure I.4: Taxonomic distribution of marine cyanobacterial natural products reported during 2010-2011 .………………………………………………….…………... 15 Figure II.1: Underwater pictures and microphotographs of cf. Oscillatoria margaritifera NAC8-46 from Curaçao ……………………………………….……………….. 39 Figure II.2: Phylogenetic inference of the tumonoic acid-producing cf. Oscillatoria margaritifera strains from Curaçao ……………………………..…................. 43 Figure II.3: Molecular structures of Ethyl tumonoate A ............................................... 47 Figure II.4: Mosher’s esters of Ethyl tumonoate A ........................................................ 49 Figure II.5. HR-ESI-MS of Ethyltumonate A ……………………..………..…............ 56 Figure II.6: 1H-NMR of Ethyltumonate A …………………………….……………… 57 Figure II.7: 13C-NMR spectrum of Ethyltumonate A ………………..……………….. 58 Figure II.8: COSY spectra of Ethyltumonate A …..………………………..…………. 59 Figure II.9: HSQC spectra of Ethyltumonate A …..………………………..…………. 60 Figure II.10: HMBC spectra of Ethyltumonate A …………………………….……… 61 Figure II.11: 1H-NMR of S-MTPA ester of Ethyltumonate A ……….………………. 62 Figure II.12: 1H-NMR of R-MTPA ester of Ethyltumonate A …………………….… 63 Figure III.1: Underwater pictures and microphotographs of Lyngbya specimens ……. 85 ix Figure III.2: Phylogenetic tree of the order Oscillatoriales ………………….…..….… 89 Figure III.3: Phylogenetic tree of the “tropical marine Lyngbya lineage” …............… 91 Figure III.4: Average pair-wise sequence divergence between 16S rRNA genes ……. 97 Figure IV.1: Phylogenetic relationships of the 59 cyanobacterial strains with sequenced genomes ………………….……………………………………………........… 120 Figure V.1: Geographic map of Curaçao …………………………...………...……… 154 Figure V.2: Secondary metabolites attributed to the genus “Lyngbya” obtained from Curaçao …………….…………………………….......……..………………… 158 Figure V.3: Phylogenetic inferences for “Lyngbya” specimens from Curaçao ........... 163 Figure V.4: Scanning/transmission electron micrograph (SEM/TEM) of the surface of a cultured “L. sordida” 3L filament colonized by heterotrophic bacteria …….………….…………………………………………………..……………. 166 Figure VI.1: Phylogenetic inferences Moorea diversification based on SSU (16S) rRNA nucleotide sequences ……………………………..........…..…………….…… 185 Figure VI.2: Phylogenomic inferences of Moorea gen. nov ………………………… 187 Figure VI.3: Phylogenetic inferences of the Moorea lineage ………………………... 189 Figure VI.4: Phylogenetic analyses of Lyngbya and Moorea diversification based on 16S-23S Internal transcribed spacer (ITS) regions ………………....………… 191 Figure VI.5: Morphological characterization of Moorea gen. nov ……...………...… 193 Figure VI.6: Microphotographs of cyanobacterial filaments obtained by transmission electron microscopy (TEM) ……………………………...…………………… 194 Figure VI.7: Phylogenetic analyses of Lyngbya and Moorea diversification based on RNA polymerase gamma-subunit (rpoC1) nucleotide sequences ...……..…… 206 x Figure VI.8: Photomicrographs of cyanobacterial filaments obtained by epifluorescent microscopy ……………………………...………………………..…………… 207 Figure VI.9: Microphotographs of cyanobacterial filaments obtained by transmission electron microscopy (TEM) ……………………………......………………… 208 Figure VII.1: Evolutionary tree of marine NP-producing cyanobacteria …….……… 225 Figure VII.2: Highlight of the lineage including tropical marine “Lyngbya” and tropical marine “Symploca” ……………………...…………………….……………… 227 Figure VII.3: Natural products from Moorea gen. nov . …………….………………. 228 Figure VII.4: Highlight of the “Trichodesmium-Oscillatoria” lineage
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