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Paraburkholderia Bacteria As Interesting Sources of Specialized Metabolites

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Paraburkholderia Bacteria As Interesting Sources of Specialized Metabolites The biotechnological potential of natural populations of Burkholderiales bacteria for antibiotic production Thesis presented for the degree of Philosophiae Doctor By Amal Saeed Alswat In candidature for the degree of Philosophiae Doctor Organisms and the Environment Division Cardiff School of Biosciences Cardiff University 10 July 2020 Summary Background. This study aimed to discover novel antibiotics produced by Burkholderia and Paraburkholderia bacteria as interesting sources of specialized metabolites. A novel collection of environmental Burkholderia and Paraburkholderia from the Bornean jungle, Sabah, Malaysia was assembled for the analysis. Methods. After evaluation of different growth media, a total of 98 environmental samples were screened for the presence of these bacteria by enrichment on Pseudomonas cepacia azelaic acid tryptamine (PCAT) medium. Molecular identification using the recA and 16S rRNA gene was performed and a total of 57 isolates were genome sequenced ahead of phylogenomic analyses. Antibiotic production by the jungle strains was evaluated using an antimicrobial antagonism overlay assay, genome mining, and high performance liquid chromatography (HPLC) analysis. Results. Over 50% of the 98 jungle samples were Burkholderia/Paraburkholderia recA PCR- positive. A total of 123 jungle isolates were purified and draft genome sequences were obtained for 57 of them. Genomic taxonomy identified that 45 isolates (85%) were within the newly described Paraburkholderia, and 13 isolates (15%) grouped within Burkholderia. Within the Paraburkholderia, 22 isolates were likely Paraburkholderia tropica, with a further 22 representing potentially novel taxa. All 12 Burkholderia isolates were members of the Burkholderia cepacia complex, including three that were likely a novel species group. The Burkholderia strains were all bioactive, but Paraburkholderia did not show antimicrobial activity under the conditions tested. Genome mining using antiSMASH showed that the capacity of Burkholderia to encode antibiotic biosynthesis gene clusters (BGCs) was greater than Paraburkholderia. Conclusions. The Bornean jungle in Sabah, Malaysia, is a rich source of Burkholderia and Paraburkholderia bacteria. Classification of these bacteria using genomic taxonomy approaches accurately identified known and novel species within the collection. The i environmental Burkholderia cepacia complex (Bcc) jungle strains were promising antimicrobial producers, however, despite their taxonomic diversity, the Paraburkholderia did not show any antimicrobial activity ii Acknowledgement I would like to express my sincere gratitude to my PhD supervisor Prof. Eshwar Mahenthiralingam for the continuous support of my PhD study, and for his patience, and motivation during my study. His valuable guidance helped me all the time of my PhD and writing of this thesis. I gratefully acknowledge the funding received towards my PhD research from Taif university, and I would like to thank the Royal Embassy of Saudi Arabia ‘Cultural Bureau’ in London for their encouragement and ultimate supports during my PhD journey. I greatly appreciate my second supervisors Prof. Andrew Weightman for giving the encouragement and sharing insightful suggestions. I am grateful to Esh lab colleagues for providing me with assistance throughout my study, especially to Dr Gordon Webster for always being so supportive of my work. I would also like to say a heartfelt thank you to my dad, mum and brothers for all the support you have shown me through this research. A very special thank you to my friends Mrs. Roaa Alnemari and Ms. Hanouf Bafhaid for helping in whatever way they could during this challenging time of my life. iii Contents General introduction and aim .......................................................................... 1 1.1 General introduction .................................................................................................... 1 1.2 Burkholderia sensu lato bacteria (1992-2020) ............................................................. 1 1.2.1 The Burkholderia genus and examples of well-described species groups within it 3 1.2.1.1 Burkholderia cepacia complex (Bcc) ............................................................... 3 1.2.1.2 Burkholderia pseudomallei group .................................................................... 6 1.2.1.3 Burkholderia gladioli group ............................................................................. 6 1.2.2 Paraburkholderia genus (2014-2020) .................................................................... 7 1.2.3 Caballeronia genus (2016 – 2020) ...................................................................... 10 1.2.4 Other genera not accommodated by the Burkholderia, Paraburkholderia and Caballeronia genera: Robbsia, Mycetohabitans and Trinickia ...................................... 10 1.3 The threat of antibiotic-resistant superbugs ............................................................... 12 1.3.1 Urgent need for new antibiotics: Burkholderia as promising novel antibiotic producers ..................................................................................................................... 13 1.4 PhD aim and objectives ............................................................................................. 15 Objective 1. Develop cultivation-based and cultivation-independent methods to screen environmental samples for the presence of Burkholderia and Paraburkholderia bacteria (Chapter 3). ................................................................. 16 Objective 2. Apply cultivation and cultivation-independent methods to detect Burkholderia bacteria in the natural environment (Chapter 4). .............................. 16 Objective 3. Identify environmental Burkholderia and Paraburkholderia species using whole-genome sequencing (WGS) and bioinformatics tools (Chapter 5). .... 17 iv Objective 4. Screen the Burkholderia and Paraburkholderia collections for the presence of novel antibiotics using bioactivity and genome-mining analysis (Chapter 6)............................................................................................................ 17 Materials and methods ................................................................................... 18 2.1 Growth cultures and chemicals .................................................................................. 18 2.2 Bacterial strains and routine growth and storage conditions ...................................... 19 2.2.1 Strains panels and bacterial samples .................................................................. 19 2.2.2 Growth and storage of bacterial isolates ............................................................. 21 2.2.3 Bacterial growth in 96-bioscreen plate and data analysis protocol ....................... 21 2.2.4 Rapid screening method for determining bacterial growth on enrichment media . 23 2.3 Sampling in Sabah and storage ................................................................................. 24 2.3.1 Reviving samples and initial screening to isolate single colonies using spiral platter technology ................................................................................................................... 25 2.4 Identification of environmental bacteria by molecular methods and bioinformatics analysis ........................................................................................................................... 25 2.4.1 DNA extraction from environmental enrichment and pure bacterial cultures ........ 25 2.4.2 The quantitation and quality assessment of DNA ................................................ 26 2.4.3 Primer design and synthesis ............................................................................... 27 2.4.4 Marker genes amplification using polymerase chain reaction (PCR) ................... 27 2.4.5 PCR purification for 16S rRNA and recA gene phylogenies ................................ 29 2.4.6 16S rRNA and recA genes sequencing and bacterial species identification using phylogenetic analysis ................................................................................................... 29 2.4.7 Whole genome sequencing and bioinformatics analysis ...................................... 30 2.5 Antimicrobial production analysis ............................................................................... 32 v 2.5.1 Screening of antimicrobial activity using antagonism assays for Jungle isolates . 32 2.5.2 Metabolite analysis by high performance liquid chromatography (HPLC) ............ 33 2.5.3 Genome mining approach by means of antiSMASH 0.0.5 and graph pad data presentation ................................................................................................................. 35 2.6 Statistical analysis ..................................................................................................... 36 Enrichment media to identify environmental Burkholderia and Paraburkholderia .............................................................................................................. 37 3.1 Introduction ................................................................................................................ 37 3.1.1 Aim and objective ................................................................................................ 38 3.2 Results ...................................................................................................................... 40 3.2.1 Bromoacetic Acid is not
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