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The Diversity and Bioactivity of Endophytes Associated With The Diversity and Bioactivity of Endophytes Associated with Medicinal Plants Used by the Dharawal People of Botany Bay !"#$%&"'()'*+)#,-."#'()+"/-$0"12)%3) 1-1$%+%1%4"*56$%+7#"*8).'$"*-)'*".'(0)) Shane David) Ingrey B.Sc (Hons.) University) of New South Wales 9%#:2);,'7) ! A thesis submitted in fulfilment of the requirements for the degree ! of! "!#$%&'&!'(!)*+)'+,%(#!-)!#$%!.%/*'.%,%(#&!)-.!#$%!0%1.%%!-)Doctor of Philosophy (Ph.D.) ! ! 2-3#-.!-)!4$'+-&-5$6! ! ! ! ! 73$--+!-)!8'-#%3$(-+-16!9(0!8'-,-+%3*+9.!73'%(3%& ! The School of Biotechnology:93*+#6!-)!73'%(3% and Biomolecular! Sciences ! The University of !New South Wales Sydney,"*1*&#!;<=> Australia ! ! March 2014 ii Supervisor Professor Brett Neilan The School of Biotechnology and Biomolecular Sciences iii Thesis-nhay dedicated-ri ngabuwulawala, babawulawala, ngabawulawala, babaawulawala, djadjawulawala mamawulawala nagun knowledgeyanha ‘mirra ngayamayangay’. Translates literally to: This thesis is dedicated to the grandmothers, grandfathers, mothers, fathers, brothers and sisters who without their knowledge ‘I would have had nothing’. (Dharawal Language). iv vi vii Abstract Aboriginal Australians have one of the oldest surviving cultures in the world today. The Dharawal people of Botany Bay were the first to encounter the British first in 1770 and again in 1788. The Dharawal use plants for a variety of reasons that also includes medicinal properties. This thesis investigates ethnobotanical information of seven medicinal plants used by the Dharawal people of Botany Bay that were provided by the Dharawal elders group and community members of the La Perouse Aboriginal community who engaged in continual cultural practice. Endophytic microorganism communities that reside within the plant tissue of each medicinal plant were organised phylogenetically based on 16S rRNA and 18S rRNA genes. The culturable endophytes that were identifiable were phylogenetically grouped within ten orders of fungi and three classes of bacteria. These endophytes were also further investigated for biosynthetic potential of natural products via genetic screening targeting enzyme encoding genes, non-ribosomal peptide synthetase (NRPS) and polyketide synthase (PKS). Endophytes that possessed NRPS or PKS encoding genes were subjected to preliminary bioassay tests against a range of bacterial and fungal test organisms. All but one showed activity against at least one test organism. Three endophytes were selected for further compound isolation. Isolation and structure elucidated of bioactive compounds from an endophytic Aspergillus sp. revealed known compounds such as triacylglycerides (SDI-63), bisabolane sesquiterpenoids (SDI-66) and a novel bioactive polyketide (SDI-69) via 1H, 13C, and 2D NMR experiments. Compound SDI-69 possessed anti-bacterial properties against S. aureus, P. aeroginosa, E. coli, C. diptheriae and B. subtilis at concentrations of 10 µg/mL or 100 µg/mL. The traditional knowledge present in today’s society has revealed that these medicinal plants provide a habitat for a diverse range of endophytic microorganisms. These endophytes contain NRPS and PKS encoding genes and produce bioactive compounds, leading to the inference of the role of endophytes and their medicinal properties in various indigenous plant species. This approach to natural product discovery will allow conservation of these medicinal plant species and the associated traditional practices to provide continual access to novel bioactive natural products produced by endophytes. v Acknowledgements I would firstly like to acknowledge all the Dharawal people of the Sydney and Botany Bay area, both past and present, whose knowledge, resilience and persistence in the face of massive change and adversity have kept our culture alive. In regards to this study, my grandmother, a proud Dharawal and Dunghutti elder, whose knowledge was an integral part of this study, not only her knowledge of medicinal plants but her traditional values and pride in continuing our culture. This shown through my father and in my brothers, sister, cousins, nieces and nephews, made this study one of the most proudest moments of my life. It’s just a shame you are not physically here to see it completed. I would also like to thank the Dharawal Elders Group for their input into this project. I would also like to pay my respects and thanks to the Aunties, my grandmother’s sisters and cousins that had been involved in the project but had passed away. I hope I did you all proud. I would like to thank my supervisor Brett Neilan for letting me hang around so long. Your supervision, friendship and mentorship during this study has not only made my time in the lab most enjoyable, but also showed me the importance of a balance of work and play. It was a privilege to work and learn from you. Co-supervisor John Kalaitzis, thank you for all your help and guidance of the years, especially in recent times with chemistry and manuscript prepping and tough topic of Rugby League. Souths vs Parra grand final? A big thank you to Professor Nakata and the team at Nura Gili for all the support and advice that you have given during this time. Alex and Alper… well I did it. We’re just waiting for you now Alper. Thanks for being such good mates during our time here. Current and former endophyte/symbiont people Kristin, Alvin, Jeff, Toby and Rocky, thanks for all the support over the years with culturing, NMR, chemistry and general advice and friendship. To all the lab members of the BGGM, past and present, thank you for all your help and all the fun memories. You have made this time a most memorable one. viii Mum and Dad thank you for all your support and patience. I really appreciate all the help and support you have always given me. Ditto Glenis and Van. I have finally finished. Yeano, Ray, Mick, Boote and Wana thanks for all the input especially from the cultural perspective. You’re all doing a good job in keeping our culture alive and moving forward. I’m very proud to have you as my siblings. Also thanks to Kez, Kobi, Shal, Clare and Aaron, Fleur, Chloe, Gordon, Dean and Vanessa. All the kids, lets hope some of you get to write one of these one day. Grandma. YAY! I finished this in your lifetime. Thank you for all your support that you have given us. Your kindness and love have made this journey much easier and I will always be grateful for everything you have done. Renee, a massive thank you for being the most patient, understanding, beautiful and loving wife a person could ask for. Without you I would not have been able to finish this. Maybe one day Olive could be doing this as well. M-A-Y-B-E. Olive I love you. (Post hand in: David I love you too) If I have forgotten anyone I am sorry and would like to apologise and thank you. My lack of sleep and excitement to hand in has got the better of me. Since I have finally finished and bought this long journey to a close, let’s hope the Rabbitohs can do the same thing and win the comp this year. (and they did!) ix List of Publications and Presentations Refereed papers • Shane D. Ingrey, John A. Kalaitzis and Brett A. Neilan. Gooris, Invaders and Modern Ethnobotany: The Evolution of Traditional Medicines from Australia. (Submitted to Journal of Ethnobiology and Ethnomedicine). • Miller K, Ingrey S, Alvin A, Sze D, Roufogalis DA, Neilan BA (2010). Endophytes and the microbial genetics of traditional medicines. Microbiology Australia (May edition): 60-3. Conference procedings • Ingrey SD, Neilan BA (2008) (Abstract). The genetic basis for bioactivity in the traditional medicine plants of Australia. Planta Medica 74:908. (DI0668388)* This abstract was accepted for a short conference talk at the 7th meeting of AFERP, ASP, GA, PSE and SIF, 2008 in Athens, Greece. This was a joint meeting of top natural products societies of Europe and America. • Miller, K. I., Ingrey, S., Sze D.M., Roufogalis, B., Qing, C., Neilan, B. (2008) Bioprospecting for Endophyte Related Natural Products in TCM Anti-Cancer Herbs. Natural Products Conference, 7th Joint Meeting of AFERP, ASP, GA, PSE and GIF, Athens, Greece. Other UNSW TV. Cloning bush medicine (2010). http://tv.unsw.edu.au/video/cloning-bush- medicine. Papers in preparation 1. Ingrey, S.D., Dharawal elders group, Miller, K., Kalaitzis, J.A., Neilan, B.A. The Microbial Diversity of Endophytes from Traditional Medicine Plants Used by the Dharawal People of Botany Bay, Sydney, Australia. 2. Ingrey, S.D., Sreekanth, D., Kalaitzis, J., Neilan, B.A. Bioactivity of Endophytes Isolated from Traditional Medicine Plants of Sydney, Australia. 3. Ingrey, S.D., Kalaitzis, J., and Neilan, B.A. Novel Polyketide Isolated from an Endophytic Aspergillius sp. and its Anti-bacterial Activity. (Proposed) x List of Abbreviations A adenylation AGA arginine/glycerol agar BLAST basic local alignment search tool bp base pairs C condensation CD3OD deuterated methanol CDCl3 deuterated chloroform COSY correlated spectroscopy DCM dichloromethane DH dehydratase DMSO dimethyl sulfoxide DMSO-d6 deuterated DMSO DNA deoxyribonucleic acid E epimerisation EDTA ethylenediamineteraacetic acid ER enoylreductase GTR general time reversible h hours HMBC heteronuclear multiple bond coherence HPLC high performance liquid chromatography HSQC heteronuclear single quantum coherence HR-ESI-MS high resolution electrospray ionisation mass spectrometry KR ketoreductase KS ketosynthase KSα ketoacyl synthase KSβ ketoacyl synthase m/z mass to charge ratio MHz megahertz MPLC medium pressure liquid chromatography MS mass spectrometry NA not available NCBI National Centre for Biotechnology Information NT not tested NMR nuclear magnetic resonance NRP non-ribosomal peptide NRPS non-ribosomal peptide synthetase OD optical density PCP peptidyl carrier protein PCR polymerase chain reaction PDA potato dextrose agar PK polyketide PKS polyketide synthase POP palmitic oleic palmitic PS plant species PUFA polyunsaturated fatty acid RDBE ring and double bond equivalent RP-HPLC reverse phase HPLC s seconds xi rRNA ribosomal ribonucleic acid SDS sodium dodecyl sulphate SEM standard error of the mean sp.
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