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Bioactive Natural Products from Marine Macroalgal Endophytes from the Bay of Fundy, Canada

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BIOACTIVE NATURAL PRODUCTS FROM MARINE MACROALGAL ENDOPHYTES FROM THE BAY OF FUNDY, CANADA by Andrew J. Flewelling BSc (Hons), University of New Brunswick, Saint John, 2010 MSc, University of New Brunswick, Saint John, 2013 A Dissertation Submitted in Partial Fulfilment of the Requirements for the Degree of Doctor of Philosophy in the Graduate Academic Unit of Biology, Saint John Supervisor: Christopher A. Gray, PhD, Departments of Biological Sciences & Chemistry Examining Board: John A. Johnson, PhD, Department of Biological Sciences Anton Feicht, PhD, Department of Biological Sciences Larry Calhoun, PhD, Department of Chemistry External Examiner: John Sorensen, PhD, Department of Chemistry, University of Manitoba This dissertation is accepted by the Dean of Graduate Studies THE UNIVERSITY OF NEW BRUNSWICK December 2017 © Andrew Flewelling, 2018 ABSTRACT We are approaching a time where antimicrobial drugs may no longer be effective due to the growing global antimicrobial resistance crisis, coupled with the lack of antimicrobial drug discovery and development. New antimicrobial therapies are needed, and endophytes from marine macroalgae have been highlighted as an important biological reservoir for the identification of novel antimicrobial molecules. A preliminary investigation of marine macroalgae from the Bay of Fundy, New Brunswick, Canada for their endophytes indicated this location to be an excellent source of endophytic fungi possessing antimicrobial activity. One hundred and forty fungal endophytes were isolated from 20 species of marine macroalgae collected from the Bay of Fundy. Fifty-four endophytes were identified to the genus or species level, and include eleven fungi not previously isolated as endophytes of marine macroalgae. The identity of 86 isolates could not be confirmed through DNA sequencing due to an inability to amplify or sequence DNA or due to low sequence homology with entries in GenBank. These isolates were designated codes according to their morphology. Each endophyte was fermented to obtain an extract in order to facilitate the discovery of new natural products. In order to prioritise the extracts obtained from these endophytic fungi, an antimicrobial bioactivity profiling technique was developed using nine microorganisms and a panel of 17 antimicrobial standards to not only attempt to identify new antimicrobial natural products, but also those that possess unique antimicrobial targets or modes of action. Principal component analysis of the extract bioactivity profiles revealed that the profiles of 37 extracts were unique within the library. Hierarchical cluster analysis using the profiles of the 37 unique extracts and the 17 antimicrobial standards showed that 26 extracts possessed bioactivity ii profiles that were distinct from the antimicrobial standards and thus warranted further investigation. Subsequent bioassay guided fractionation of four fungal extracts led to the isolation of six antimicrobial natural products: penicillic acid, methylenolactocin, fumagillin, fumigatin oxide, poly(3R,5R-dihydroxyhexanoic acid) and (P/M)- maximiscin. These natural products, while being known chemical entities, are all reported to possess antimicrobial activity and may play an important role in future antimicrobial drug discovery and development. iii DEDICATION To my family and friends, for all of their support. iv ACKNOWLEDGEMENTS I must start off by thanking my mentors, Dr. Christopher Gray and Dr. John Johnson, for their commitment, valued support and guidance given to me over the last eight years, and especially the last five for my PhD. I consider myself extremely fortunate to have had the opportunity to work with you and to have had the memorable experiences that being a member of the Natural Products Research Group has given me. I can certainly say that without your advice and support, both personal and professional, I would not have made it to this point in my studies. I would also like to thank Dr. Christopher Martyniuk for serving on my supervisory committee. I truly appreciate the advice and time given to me for the development and completion of this thesis. I must acknowledge the generous support provided by Dr. Russell Kerr and Dr. Hebelin Correa, UPEI, and Dr. Larry Calhoun, UNB. Their respective work in obtaining mass spectroscopy and NMR data for my samples is greatly appreciated. Also, I must thank Dr. Gilles Robichaud and Roxann Guerrette, UdeM, for their willingness to acquire cytotoxicity data for my samples. I would also like to thank Dr. Thierry Chopin, UNBSJ, for identifying the macroalgae collected. I would especially like to acknowledge the work performed by Kelsey Pendleton in isolating the endophytic fungi. Her work was invaluable for the completion of this thesis. There are several colleagues from the Natural Products Research Group, past and present that continually contributed both directly and indirectly to my research: Allyson Bos, Trevor Clark, Haoxin Li, and Taryn O’Neill. I have extremely enjoyed working with v all of you and am eternally grateful for the support you have given me. To Ally and Trevor, I will not forget the amazing “work” we did in South Africa. Finally, I must thank my family and friends for their endless support. To my parents, Marilyn and Gerry: I am the luckiest guy in the world. You have been there every step of the way and have given me unconditional support. I know I wouldn’t have made it through this degree without you – thank you. vi TABLE OF CONTENTS ABSTRACT ...................................................................................................................... ii DEDICATION ................................................................................................................. iv ACKNOWLEDGEMENTS .............................................................................................. v TABLE OF CONTENTS ................................................................................................ vii LIST OF TABLES .......................................................................................................... xii LIST OF FIGURES ........................................................................................................ xv LIST OF ABBREVIATIONS ........................................................................................ xix Chapter 1: General introduction ........................................................................................ 1 1.1 The need for new antimicrobial therapies .......................................................... 2 1.2 Natural products as a source for new antimicrobials ....................................... 11 Chapter 2: Isolation and identification of endophytes from marine macroalgae of the Bay of Fundy, Canada ............................................................................................................ 14 2.1 Introduction ...................................................................................................... 15 2.1.1 Endophytic fungi from marine macroalgae .............................................. 15 2.1.2 Rationale for investigating marine macroalgae from the Bay of Fundy, New Brunswick, Canada for endophytic fungi ............................................................... 19 2.2 Experimental .................................................................................................... 20 2.2.1 Media composition .................................................................................... 20 2.2.2 Algal collection ......................................................................................... 20 2.2.3 Surface sterilization of algae ..................................................................... 21 2.2.4 Culture techniques .................................................................................... 23 2.2.5 Isolation of endophytic fungi .................................................................... 24 vii 2.2.6 Cryopreservation of endophytic fungi ...................................................... 25 2.2.7 Identification of endophytic fungi............................................................. 26 2.2.8 Statistical analyses .................................................................................... 28 2.4 Results and discussion ...................................................................................... 28 2.5 Conclusions ...................................................................................................... 48 Chapter 3: Development of a simple bioactivity profiling technique for the prioritization of a library of extracts from endophytes of marine macroalgae of the Bay of Fundy, New Brunswick, Canada ......................................................................................................... 49 3.1 Introduction ...................................................................................................... 50 3.2 Experimental .................................................................................................... 52 3.2.1 Liquid culture fermentation ...................................................................... 52 3.2.2 Preparation of extracts .............................................................................. 52 3.2.3 Preparation of antimicrobial standards for bioactivity profiling data set.. 53 3.2.4 Antifungal activity assay ........................................................................... 53 3.2.5 Antibacterial activity assay ......................................................................
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