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Isolation and Characterization of a Sponge-Associated Actinomycete That Produces Manzamines

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Isolation and Characterization of a Sponge-Associated Actinomycete That Produces Manzamines ABSTRACT Title of Document: ISOLATION AND CHARACTERIZATION OF A SPONGE-ASSOCIATED ACTINOMYCETE THAT PRODUCES MANZAMINES Olivier Peraud, Doctor of Philosophy, 2006 Directed By: Professor Russell T. Hill Marine Estuarine Environmental Sciences Two Indonesian sponges, Acanthostrongylophora sp. Sponge 35 and Sponge 52, containing manzamine A were collected off the coast of Manado, Indonesia. Manzamines are a family of marine alkaloids that exhibit a complex molecular architecture and possess bioactivities including antitumour, antimicrobial, antiparasitic and insecticidal activities. Manzamines have been found in 17 different species of sponges with wide geographical distribution which has led to speculation that they may be produced by a microbial symbiont rather than by the sponges themselves. The sponges’ microbial communities were investigated using 16S rRNA gene analysis and a rational culture-based microbiology approach in which specific bacterial groups were targeted. The molecular analysis of these microbial communities revealed that they were complex and diverse. Microbiological analyses were conducted on Acanthostrongylophora sp. with a particular emphasis on the isolation of actinomycetes because of the high number of actinomycete sequences in this sponge 16S rRNA gene clone library and their excellent track record as bioactive compound producers. One of the isolated actinomycetes, Micromonospora sp. strain M42, produces manzamine A and 8-hydroxy-manzamine, compounds initially detected in the sponge. A detailed analysis of Micromonospora sp. strain M42 showed that it grew on a wide range of salt concentrations with an optimal growth at 0-1% NaCl. Cultures of Micromonospora sp. strain M42 consistently produced manzamine A with a maximum yield of 1 mg/l. The genome size of Micromonospora sp. strain M42 was estimated at 6.7 Mb by pulsed field gel electrophoresis. The biosynthetic gene pathway encoding manzamine A was investigated using both biochemistry and molecular methods yet it remains elusive. Micromonospora sp. strain M42 underwent UV mutagenesis leading to isolation of mutants with yield of manzamine A improved by 3.5 fold. One of the mutants produces manzamine B, the putative biosynthetic precursor of manzamine A. A fosmid library of Micromonospora sp. strain M42 was constructed and low-pass genome sequencing gave insights into the strain’s genome and revealed a high number of genes devoted to the production of secondary metabolites including polyketides and non-ribosomal peptides. The isolation of Micromonospora sp. strain M42 greatly improves the chances of manzamines becoming a drug class for treatment of malaria. ISOLATION AND CHARACTERIZATION OF A SPONGE-ASSOCIATED ACTINOMYCETE THAT PRODUCES MANZAMINES By Olivier Peraud Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2006 Advisory Committee: Professor Russell T. Hill, Ph.D., Chair Professor Mark T. Haman, Ph.D. Professor Frank T. Robb, Ph.D. Professor Feng Chen, Ph.D. Assistant Investigator Jacques Ravel, Ph.D. © Copyright by Olivier Peraud 2006 Dedication This dissertation is dedicated to my parents, Jeannine and Michel ii Statement of Contribution Dr. K. V. Rao (University of Mississippi) performed the manzamine assays on samples from Micromonospora sp. strain M42 cultures. Ms. Jennifer Allman (University of Mississippi) assisted in providing figures of the molecular structures. Mr. Matthew Anderson (Center of Marine Biotechnology) mutated Micromonospora sp. strain M42 and screened the mutants for hyperproducing mutants. Dr. Jacques Ravel (The Institute for Genomic Research) contributed to the construction of Micromonospora sp. strain M42 fosmid library. The sequencing of Micromonospora sp. strain M42 fosmid library was done at TIGR thanks to Dr. Ravel who also helped in the sequence analysis. iii Acknowledgements I would like to thank my advisor, Russell Hill who gave me the opportunity to work on this truly exciting research project. He has been a great help all along and taught me discipline and rigor in my work. Russell greatly improved my English both in speech and writing. I enjoyed our arguments and the fact that I was always treated as a colleague even when I was a junior graduate student. Finally, Russell, thank you for having been there when I had difficult times, especially at the beginning. Next, I would like to thank my committee members, Mark, Frank, Feng and Jacques who have always been very accessible and contributed greatly to this work with their suggestions and analyses. I would like to especially thank Jacques Ravel for his help and also for having listened to me complaining in French. Playing table tennis at TIGR was lots of fun and perhaps I will beat you someday. Matthew Anderson has been very involved in this project and carried out the mutation studies of Micromonospora sp. strain M42. Thank you for your help and for putting up with all my always urgent last minute requests. I would also like to thank Julie Enticknap. She’s been a good friend and her stories were always a laugh. iv Table of Contents Dedication........................................................................................................................... ii Statement of Contribution..................................................................................................iii Acknowledgements............................................................................................................ iv Table of Contents................................................................................................................ v List of Tables ...................................................................................................................viii List of Figures.................................................................................................................... ix List of Abbreviations .......................................................................................................xiii 1 Introduction................................................................................................................. 1 1.1 Sponges............................................................................................................... 1 1.1.1 Sponge biology........................................................................................... 2 1.1.2 Sponge taxonomy........................................................................................ 3 1.1.3 Sponge microbiology.................................................................................. 6 1.2 Marine natural products ...................................................................................... 9 1.2.1 The “supply problem”............................................................................... 11 1.2.2 Natural products from sponge-associated bacteria ................................... 11 1.2.2.1 Actinomycetes....................................................................................... 11 1.2.2.2 Pseudomonas/Alteromonas................................................................... 16 1.2.2.3 Pseudoalteromonas............................................................................... 21 1.2.2.4 Flexibacter ............................................................................................ 21 1.2.2.5 Roseobacter/Ruegeria........................................................................... 22 1.2.2.6 Cyanobacteria ....................................................................................... 24 1.2.2.7 Vibrio .................................................................................................... 27 1.2.2.8 Sponge metabolites of likely bacterial origin ....................................... 28 1.2.2.9 Future approaches................................................................................. 30 1.3 The actinomycetes ............................................................................................ 32 1.3.1 Ecology of actinomycetes......................................................................... 33 1.3.2 Sponge-associated actinomycetes............................................................. 35 1.3.3 Secondary metabolites .............................................................................. 36 1.3.4 The genus Micromonospora ..................................................................... 37 1.3.4.1 Description of the genus Micromonospora........................................... 37 1.3.4.2 Bioactive metabolites from marine Micromonospora .......................... 38 1.4 Manzamines ...................................................................................................... 40 1.4.1 Manzamine A............................................................................................ 41 1.4.1.1 Biogenic pathway..................................................................................41 1.4.1.2 Pharmacology of manzamine A............................................................ 41 1.5 Bacterial genomics............................................................................................ 43 1.5.1 Application of genomics to the identification of bioactive compounds ... 44 1.5.2 The polyketides......................................................................................... 46 1.5.2.1 General background.............................................................................
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