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Actinobacterial Diversity in Atacama Desert Habitats As a Road Map to Biodiscovery

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Actinobacterial Diversity in Atacama Desert Habitats As a Road Map to Biodiscovery Actinobacterial Diversity in Atacama Desert Habitats as a Road Map to Biodiscovery A thesis submitted by Hamidah Idris for the award of Doctor of Philosophy July 2016 School of Biology, Faculty of Science, Agriculture and Engineering, Newcastle University, Newcastle Upon Tyne, United Kingdom Abstract The Atacama Desert of Northern Chile, the oldest and driest nonpolar desert on the planet, is known to harbour previously undiscovered actinobacterial taxa with the capacity to synthesize novel natural products. In the present study, culture-dependent and culture- independent methods were used to further our understanding of the extent of actinobacterial diversity in Atacama Desert habitats. The culture-dependent studies focused on the selective isolation, screening and dereplication of actinobacteria from high altitude soils from Cerro Chajnantor. Several strains, notably isolates designated H9 and H45, were found to produce new specialized metabolites. Isolate H45 synthesized six novel metabolites, lentzeosides A-F, some of which inhibited HIV-1 integrase activity. Polyphasic taxonomic studies on isolates H45 and H9 showed that they represented new species of the genera Lentzea and Streptomyces, respectively; it is proposed that these strains be designated as Lentzea chajnantorensis sp. nov. and Streptomyces aridus sp. nov.. Additional isolates from sampling sites on Cerro Chajnantor were considered to be nuclei of novel species of Actinomadura, Amycolatopsis, Cryptosporangium and Pseudonocardia. A majority of the isolates produced bioactive compounds that inhibited the growth of one or more strains from a panel of six wild type microorganisms while those screened against Bacillus subtilis reporter strains inhibited sporulation and cell envelope, cell wall, DNA and fatty acid synthesis. Initial culture-independent studies were carried out to establish the extent of actinobacterial diversity in a range of hyper- and extreme hyper-arid Atacama Desert soils. Community DNA extracted from soil collected from the sampling sites was surveyed for actinobacteria by 454 pyrosequencing; rarefaction analyses indicated good coverage at most of the sites. The results revealed an amazing and unexpected taxonomic diversity at the ranks of order, family and genus, much of it novel. The total number of genera, for instance, is 328, of which around 40% could not be assigned to validly published genera. Rank abundancy profiles indicated that much of this diversity can be attributed to low abundancy taxa. Similar results were obtained from community DNA extracted from surface and subsurface soil samples collected at three different altitudes on Cerro Chajnantor. Actinobacterial community structure at these sampling sites was influenced by altitude and sampling depth, as well as several environmental variables that included conductivity, pH, redox potential and organic matter content. It is evident from these studies that the Atacama Desert landscape abounds in novel actinobacterial taxa that synthesize a broad range of specialized metabolites that can be developed as drug leads. i Author’s Declaration Except where acknowledgement has been given, this dissertation is the original work of the author. The material presented has never been submitted to the Newcastle University or to any other educational establishment for purposes of obtaining a higher degree. July 2016 Hamidah Idris ii Acknowledgements First and foremost I would like to thank my supervisor, Professor Michael Goodfellow for his support and commitment throughout my studies in Newcastle- his patience and understanding are much appreciated. Indeed, without his support and encouragement both during the experimental work and preparation of this thesis, the completion of the project may will be remained a dream. I am also grateful to my second supervisor, Dr. Ian Singleton, and my panel members, Drs. Jem Stach, and Gordon Beakes for their invaluable help with aspects of the project. My sincere thanks also go to Professor Alan Bull (University of Kent, UK), Professor Marcel Jaspar (University of Aberdeen), Professor Martha Trujillo (University of Salamanca, Spain), Professor Jongsik Chun (Seoul National University, Korea), Dr. David Labeda (National Centre for Agriculture-Utilization Research, Preroria, USA), Dr. Mostafa Rateb (University of Aberdeen), Dr. Wael Houssein (University of Aberdeen), Dr. Maria del Carmen Montero-Calassanz (Newcastle University), Dr. Imen Nouioui (Newcastle University), Dr. Roy Sanderson (Newcastle University) and Dr. Jean Franco Castro (University of Chile). I am also grateful to Mr. Owajiogak Hayford, Miss Yvonne Wu and Miss Arailym Ziyat (M.Sc. students, School of Biology, Newcastle University) for their contributions to what has turned out to be an exactly collaborative venture; their contributions are highlighted in Acknowledgements in the relevant chapters. I owe a deepest gratitude to Mrs. Roselyn Brown, Mrs. Miriam Earnshaw, Mr. Matthew Peake and Miss Kirsten Wyness for their help, support, tips and tricks, not only in laboratory work but also in sharing life experiences. I would like to thank my colleagues from the laboratory and postgraduate office, Kanungnid Busarakam and Iain Douglas for guidance with my experimental work and to my colleagues Jodel Symington, Sophie Derveau, Eli Patterson, Nadeer Fazaa for all the help and support. I am also indebted to School of Biology, especially Dr. Gordon Port, Ms. Jan Fife, Mr. Mark Bendall, Ms. Sarah Thompson, Ms. Kerry Harvey and Mr. David Moir for their much appreciated kindness and help. Special thanks go to my friend, Siti Nabilah and Ras Azira for helping me in the final phases of assembling this thesis. This thesis and my whole PhD project would not have been possible without the financial support from the Ministry of Higher Education Malaysia for a scholarship and my employer, Universiti Pendidikan Sultan Idris, Malaysia for the living allowance for my family. I am indebted to my dear husband, Zuhaili Fikri, our beloved daughter Haifa Qaisara and our newborn baby Hana Malaika for being my pillar of strength throughout our time in the lovely city of Newcastle upon Tyne. Last but not least, a million thanks to our family members in Malaysia, especially to my parents for their continuous support; it is my pleasure to dedicate my achievements to them. iii Publications Related to the Thesis Publication: Dominik Wichner, Hamidah Idris, Wael E. Houssen, Andrew R. McEwan, Alan T. Bull, Juan A. Asenjo, Michael Goodfellow, Marcel Jaspars, Rainer Ebel, and Mostafa E. Rateb (2016). Isolation and anti-HIV-1 integrase activity of Lentzeosides A-F from extremotolerant Lentzea sp. H45, a strain isolated from a high altitude Atacama Desert soil. Journal of Antibiotics (in press). Poster presentations: H. Idris, A.T. Bull, M.E. Rateb, M. Jaspars and M.Goodfellow (2013). Actinobacterial diversity in high altitude Atacama Desert soils and regoliths and its biotechnological potential. Bergey’s International Society for Microbial Systematic(BISMiS) Conference. Edinburgh, UK. H. Idris, A.T. Bull, M.E. Rateb, M. Jaspars and M.Goodfellow (2014). Actinobacterial diversity in high altitude Atacama Desert soils as sources of novel specialized metabolites. XVII International Symposium on the Biology of Actinomycetes. Kusadasi, Turkey. R. Brown, H. Idris, I. Singleton, A.T. Bull and M. Goodfellow (2014). Microbial life at high altitude: Actinobacterial diversity of surface and subsurface environmental samples from the Atacama Desert. XVII International Symposium on the Biology of Actinomycetes. Kusadasi, Turkey. iv Table of Contents Abstract ............................................................................................................................ ii Author’s Declaration ...................................................................................................... ii Acknowledgements ......................................................................................................... iii Publications Related to the Thesis ................................................................................ iv Table of Contents ............................................................................................................ v Chapter 1. General Introduction ................................................................................... 1 1.1 Background ............................................................................................................ 1 1.2 Objectives and content of thesis ........................................................................... 4 1.3 Biodiversity, bioprospecting and biogeography ................................................. 7 1.4 Unexplored actinobacterial diversity as a taxonomic roadmap to drug discovery .................................................................................................................... 11 1.4.1 Habitat selection ............................................................................................. 11 1.4.2 Selective isolation of actinobacteria from natural habitats ............................ 12 1.4.3 Pretreatment of environmental samples ......................................................... 13 1.4.4 Choice of selective isolation media................................................................ 14 1.4.5 Colony selection ............................................................................................. 15 1.4.6 Dereplication of isolates ................................................................................
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