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Transcriptomic Studies of the Bacterium Rhodobacter Capsulatus

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Transcriptomic Studies of the Bacterium Rhodobacter Capsulatus Transcriptomic studies of the bacterium Rhodobacter capsulatus by Marc Grüll, BSc A Thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology Faculty of Science Memorial University of Newfoundland St. John’s, Newfoundland and Labrador, Canada February 2019 Abstract Rhodobacter capsulatus is a purple, non-sulfur alpha-proteobacterium that is studied for different aspects of physiology and its ability to produce the bacteriophage like particle called gene transfer agent (RcGTA). These particles are capable of transferring ~4 kb of random host DNA to other R. capsulatus through a process analogous to transduction. The genes that encode the RcGTA particles are located in a region of ~15 kb called the RcGTA structural gene cluster. The exact regulatory mechanisms involved in the production of RcGTA remain elusive. I investigated the regulation of GTA regulatory genes on a global scale using next generation sequencing methods. I performed investigations to analyse small RNA (sRNA) sequences genome- wide using RNA sequencing. I compared an R. capsulatus wild-type strain to a ctrA null mutant due to previous studies that suggested the global response regulator CtrA might controll a sRNA that regulates RcGTA gene expression. Using the latest bioinformatic approach, 422 putative sRNAs were detected in R. capsulatus during early stationary phase. To get a more detailed insight into the expression of the RcGTA structural gene cluster I performed total RNA sequencing on a RcGTA overproducer mutant strain of R. capsulatus. The previously developed differential RNA sequencing (dRNA-seq) protocol, which can distinguish between primary and processed transcripts, has been modified to identify transcription start sites (TSS) and to predict transcription termination sites (TTS). The combination of total RNA and 5’ -3’ specific sequencing data allowed for the prediction of transcriptional units and to analyze operon complexity in R. capsulatus. The analysis revealed a complex operon architecture, similar to other bacterial species, with i operons having multiple TSS and TTS, genomic regions of high transcriptional activity and novel transcripts. Finally, to gain further insight into how RcGTA-associated genes affect each other, I performed qPCR experiments on eight RcGTA-associated genes within and outside of the RcGTA structural gene cluster and within five different R. capsulatus mutant strains. The results indicate that the absence of any one of the known and putative GTA regulators investigated can have effects on the transcription of GTA loci. ii Acknowledgements Many people have helped and supported my thesis research. First and foremost, I would like to acknowledge my supervisors Dr. Andrew S. Lang and Dr. Martin E. Mulligan for their continuous guidance, patience and mentorship. They always gave me a new perspective to look at experiments and challenged me to think outside of my comfort zone. Their interest and accessibility as well as their involvement and support made my research possible. I would also like to thank my co-supervisor Dr. Lourdes Peña-Castillo for her continuous involvement in my various research projects. Her efforts in the bioinformatic aspects of my research made a lot of the analysis that was performed possible and she was always thriving to improve the quality of the analysis in every aspect. I would like to thank all members, current and alumni, of the Lang lab for their help in times of crisis. The positive attitude of every lab member always made my stay in the Lang lab more than enjoyable. I would like to make a special mention of Maggie McGuire, who was my anchor and soulmate outside of the lab. Finally, I must thank my family who has supported me throughout my career. They made it possible for me to start university and move on to greater things in Canada. Although it has not always been easy to be separated by such a great distance, their continued interest in my work and mental support have made me the person and researcher that I am today, and I am forever grateful to them. My doctoral program and the research I have performed has been supported by a graduate student fellowship from the Memorial University School of Graduate Studies, and by a grant from the Dean of Science to Dr. M. Mulligan. The research in Dr. Lang’s iii laboratory was supported by grants from the Natural Sciences and Engineering Research Council (NSERC). iv Table of Contents Abstract ................................................................................................................................. i Acknowledgements ............................................................................................................ iii Table of Contents ................................................................................................................. v List of Tables ...................................................................................................................... ix List of Figures ...................................................................................................................... x List of Abbreviations, Symbols and Nomenclature ......................................................... xiii List of Appendices ............................................................................................................ xiv Co-authorship statement ................................................................................................. - 1 - Chapter 1 – Introduction and Overview .......................................................................... - 2 - 1.1 Horizontal gene transfer ................................................................................... - 2 - 1.2 Bacteriophages and prophages ......................................................................... - 4 - 1.3 Phage-like gene transfer agents (GTAs) .......................................................... - 6 - 1.4 Rhodobacter capsulatus and RcGTA ............................................................... - 8 - 1.5 Distribution of known gene transfer agents ................................................... - 12 - 1.6 RNAs and their involvement in bacterial gene regulation ............................. - 14 - 1.7 Next-generation sequencing and transcriptomics .......................................... - 21 - 1.8 Research goals ................................................................................................ - 22 - 1.9 References ...................................................................................................... - 24 - Chapter 2 - Genome-wide identification and characterization of small RNAs in Rhodobacter capsulatus and identification of small RNAs affected by loss of the response regulator CtrA ............................................................................................................... - 32 - Abstract ..................................................................................................................... - 32 - v 2.1 Introduction ......................................................................................................... - 33 - 2.2 Materials and Methods ........................................................................................ - 38 - 2.2.1 R. capsulatus growth and RNA isolation ..................................................... - 38 - 2.2.2 Library preparation and sequencing ............................................................. - 39 - 2.2.3 Processing of RNA-seq data ......................................................................... - 39 - 2.2.4 Detection of sRNAs from RNA-seq data ..................................................... - 40 - 2.2.5 Collection and analysis of sRNAs from other bacterial species ................... - 40 - 2.2.6 Bioinformatic analysis of sRNAs ................................................................. - 40 - 2.2.7 Detection of sRNAs by Northern blotting .................................................... - 43 - 2.3 Results and discussion ......................................................................................... - 45 - 2.3.1 Sequencing and detection of R. capsulatus sRNAs ...................................... - 45 - 2.3.2 sRNAs with predicted functions or homologs .............................................. - 45 - 2.3.3 Bioinformatic characterization of putative sRNAs in R. capsulatus ............ - 49 - 2.3.4 Identification of a putative tRNA-derived sRNA locus ............................... - 55 - 2.3.5 Functional and protein-interaction enrichment of potential cis-targets of putative antisense and partially overlapping sRNAs .................................... - 58 - 2.3.6 Effects of loss of ctrA on sRNA expression ................................................. - 59 - 2.3.7 Experimental validation of putative sRNAs using Northern blot analysis ... - 60 - 2.4 Conclusion ........................................................................................................... - 66 - 2.5 References ........................................................................................................... - 67 - Chapter 3 - Operon complexity in Rhodobacter capsulatus revealed by integration of total and end-targeted RNA-seq data .................................................................................... - 71 - Abstract ....................................................................................................................
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