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Download The ANALYSIS OF DNA UPTAKE BIASES IN BACTERIA WITH AND WITHOUT UPTAKE SPECIFICITY by Marcelo Andrés Mora Rodríguez M.Sc. University of Northern British Columbia, 2012 Licentiate, Pontificia Universidad Católica del Ecuador, 2006 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) December 2020 © Marcelo Andrés Mora Rodríguez, 2020 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, the dissertation entitled: Analysis of DNA uptake biases in species with and without uptake specificity submitted by Marcelo Mora in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Zoology Examining Committee: Rosemary Redfield, Zoology Supervisor Matthew Pennell, Zoology Supervisory Committee Member Sarah Otto, Zoology University Examiner Steve Hallam, Microbiology and Immunology University Examiner ii Abstract DNA uptake is the first step in natural transformation of bacteria, leading to DNA internalization and recombination. It is, therefore, a key determinant in genome evolution. Most bacteria take up DNA indiscriminately, but in Pasteurellaceae and Neisseriaceae, the uptake machinery binds preferentially to short sequences enriched in their genome, called DNA uptake signal sequences (USS or DUS). This enrichment is responsible for bacteria preferentially taking up DNA from close relatives, called ‘self-specificity’. My study’s goal was to characterize factors influencing uptake bias across the genome (chapter 2), as well as determined if uptake biases were present in a species without self-specificity (chapter 3). Chapter 2 describes my genome-wide analysis of DNA uptake by Haemophilus influenzae, a species with strong uptake bias, using both measured uptake and the predictions from a simulation model of DNA uptake. Genomic maps of DNA uptake were developed by recovering DNA after it was taken up and deep sequencing it, using DNA preparations sheared into small (50-800 bp) and large (1.5-17 kb) fragment sizes. For short donor DNA fragments, I found a strong uptake bias, up to 1000-fold, that was proportional to the similarity of the USSs to the consensus, including in DNA topology features. I found no evidence of an effect on uptake of non-USS sequences. Uptake of large donor DNA fragments had much less variation than short fragments, with 90% of genomic positions having uptake within 2-fold of the mean. However, it was difficult to assess the USS-dependent factors responsible for this variation because of stochastic noise arising from intrinsic biases of the DNA sequencing process. Chapter 3 describes an analysis to determine if uptake biases are present in Acinetobacter baylyi, a species without self-specificity. This was done by sequencing a degenerate region of synthetic DNA fragments, recovered after uptake by competent A. baylyi cells. Recovered fragments had the same sequence distribution as input DNA, which suggests that there is no evidence of uptake biases. iii Lay Summary Some bacteria can take up DNA from the environment. A few species of these bacteria prefer DNA fragments that have a short sequence pattern, called uptake sequences. These sequences are found at higher frequency than expected by chance in their own genomes and as a consequence, these bacteria preferentially take up DNA from their own species. The first goal of this study was to identify the factors responsible for the differences in uptake of regions in the genome of Haemophilus influenzae, a species that prefers its own DNA. I found that uptake depended strongly on the sequence, distribution, and DNA shape of uptake sequence. The second goal was to determine if uptake preferences are found in all species or only the ones that prefer their own DNA. No preferences were detected in uptake of DNA fragments taken up by Acinetobacter baylyi, a species that can take up DNA from different species. iv Preface Chapter 1, 3 and 4 were written by Marcelo Mora (MM). Chapter 2 was written by MM and Rosie Redfield (RR) with suggestions from Joshua Mell Chang (JM), Garth Ehrlich (GE), and Rachel Ehrlich (RE). Chapter 2: A version of this material has been published in the iScience journal as: Mora, M.; Mell Chang, J.; Ehrlich, G. D.; Ehrlich, R.L.; Redfield, R.J. Genome-wide analysis of DNA uptake by naturally competent Haemophilus influenzae. ISCIENCE (2021), doi: https://doi.org/10.1016/j.isci.2020.102007 Experimental design was conceived by JM and RR. MM conducted the uptake experiments. Sequencing of recovered and input DNA was done by JM. Sequencing of the Haemophilus influenza PittGG genome was done by GE and RE. Alignment of NP recovered DNA was done by JM. Alignment of PittGG was done by MM with scripts from JM. USS scores were calculated by MM using scripts from JM. Predictive uptake models were designed and scripted by MM and RR. Figure 2.3, 2.4, 2.15A were made by RR. The rest of figures and bioinformatic analysis were made by MM, with guidance from RR. Chapter 3: Experimental design was conceived by JM and RR. MM conducted the uptake experiments. Synthetic fragments were designed by MM, with guidance from RR and JM. Sequencing was done by the UBC Bioinformatic consortium. Bioinformatic analysis were designed and done by MM, with guidance from RR. v Table of Contents Abstract ................................................................................................................................. iii Lay Summary ......................................................................................................................... iv Preface .................................................................................................................................... v Table of Contents ................................................................................................................... vi List of Tables .......................................................................................................................... ix List of Figures .......................................................................................................................... x List of Abbreviations ............................................................................................................. xiv Acknowledgements ............................................................................................................... xv Dedication ............................................................................................................................ xvi CHAPTER ONE ......................................................................................................................... I General Introduction ............................................................................................................... I What is natural transformation and why is it important? ................................................................. I DNA uptake as part of the natural transformation process .............................................................. 2 Self-specificity and uptake sequences .............................................................................................. 4 Protein-DNA interactions ................................................................................................................. 9 Main questions about uptake bias and self-specificity .................................................................... 10 CHAPTER TWO ...................................................................................................................... 13 Genome-wide analysis of DNA uptake across the outer membrane of naturally competent Haemophilus influenzae ........................................................................................................ 13 Introduction ................................................................................................................................... 13 Direct measures of DNA uptake bias: ................................................................................................................ 15 Evolution of uptake sequences in the genome: ................................................................................................ 16 Methods ......................................................................................................................................... 18 vi Results ........................................................................................................................................... 24 A computational model of DNA uptake ............................................................................................................. 24 Model results: .................................................................................................................................................... 27 Generation of experimental DNA uptake data .................................................................................................. 30 Removal of contaminating Rd DNA: .................................................................................................................. 31 Uptake ratios: .................................................................................................................................................... 32 Sensitivity is limited by low sequencing coverage: ...........................................................................................
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