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Profiling Infectious Disease Via Single-Cell and Single-Molecule

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Profiling Infectious Disease Via Single-Cell and Single-Molecule PROFILING INFECTIOUS DISEASE VIA SINGLE-CELL AND SINGLE-MOLECULE SEQUENCING A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Philip Smith Burnham May 2019 © 2019 Philip Smith Burnham PROFILING INFECTIOUS DISEASE VIA SINGLE-CELL AND SINGLE-MOLECULE SEQUENCING Philip Smith Burnham, Ph. D. Cornell University 2019 The global burden of infectious disease has declined in recent decades. Yet, patients who are immunocompromised and individuals in resource-limited settings remain at high risk of infection. In this dissertation, I will present several next generation sequencing assays that we have created that enable new ways to monitor and study infectious diseases. I will present two classes of technologies that target two different analytes: (1) cell-free DNA (cfDNA) in biological fluids and (2) viral transcripts within single cells. We have developed a library preparation assay that is sensitive to ultrashort cfDNA, which captures information about the pathogen and host. We applied this cfDNA sequencing assay to a large number of urine samples collected from patients with viral and bacterial urinary tract infections. Our findings indicate cfDNA sequencing can accurately detect a broad range of uropathogens and describe functional information about the infectious agent and host. We have also developed a complementary analytical pipeline to reduce false-positive identifications and background contamination. We have recently applied this pipeline in the monitoring of infectious diseases that are endemic in low-income countries. Using DNA sequencing, we proved that genome replication dynamics can be observed during MTB infections and that an abundance of enteric bacteria is present in the plasma of children suffering environmental enteropathy. In the second part of the dissertation, I will introduce a new high-throughput single-cell RNA sequencing tool that combines enrichment measurements of targeted RNA sequences with unbiased profiling of the polyadenylated transcriptome across thousands of single cells in the same biological sample. We applied this technique to simultaneously characterize the non-A-tailed transcripts of a segmented dsRNA viruses and the transcriptome of the infected cells. In addition, we applied the technology to simultaneously determine the natively paired, variable region heavy and light chain amplicons and the transcriptome of B lymphocytes. In summary, we have created new tools to capture and sequence nucleic acids in biological fluids and single cells, thereby providing novel ways to understand pathogens as well as host immunity and damage. BIOGRAPHICAL SKETCH Phil was born in Philadelphia, PA in 1991. He was inspired to become a scientist by his mother. He fell in love with physics and mathematics in high school (Seneca High School, Tabernacle, NJ) and undergraduate studies (Villanova University, Villanova, PA). He began his graduate work at Cornell University to obtain a doctorate in physics in 2013. Following the start of the West Africa Ebola outbreak, he was moved to pursue the development of novel methods to understand and diagnose microbial pathogens. In the future he hopes to become a leader in understanding cellular identity within the context of environmental and community influences, particularly as it relates to infection. v This manuscript is dedicated to my family. vi ACKNOWLEDGMENTS My research progress over the past several years would not have been possible without the guidance and leadership of Iwijn De Vlaminck. Iwijn’s vision to become a leader in diagnostics and genomics first drew me to join his lab. It has been a privilege to have helped in starting the lab and to have watched it grow and evolve since 2015. My family has always encouraged my interests, pursuits, passions, and general love of science. Foremost I thank my wife, Melanie Burnham, who has constantly supported my career as a scientist. Even when research is daunting, she motivates me to achieve at the highest level. I thank my mother and Adhoedha, Elizabeth and Eric Jolly, for their support, guidance, and dedication to education and equity. My mom has encouraged me to pursue work that will leave a positive impact on the world. My Adhoedha has helped me recognize that the science is not just the act of discovery but those who are performing it. I thank my grandmother, Carole Robertson, who has always been my biggest fan. She reminds me of the importance of dreams. I thank my brother, Michael Burnham, and sister, Victoria Jolly. They have always pushed me to be a better person. I thank my father and stepmother, Phil and Diane Burnham; my aunt and uncle, Peggy Anne and Manny D’Alessio, and my cousins; and my in-laws, Todd, Betty, and Kelsey Berger. Lastly, I thank my grandfather, Henry Freda, for all he did to shape my appreciation for life. I would not have made it through my degree without the support of Hao Shi, Andre Frankenthal, Ti-yen Lan, and Archishman Raju. They have shown true friendship when life or research have been overwhelming and have become family over the past six years. They have made me think critically about both scientific and social problems. The members of the De Vlaminck lab have been instrumental in the success of my projects. I would especially like to thank: Alexandre Pellan Cheng for his friendship and shared interest in cell-free DNA and diagnostics; Mridusmita Saikia, for her guidance in the lab and for sharing her joy in experimental biology; Joan Sesing Lenz, for her support in experimental aspects; and my mentees, Sara Keshavjee, vii Michael Heyang, and Fanny Chen, for their drive and compassionate pursuits. One of the greatest parts of my research career so far has been in training and working with Sara, Michael, and Fanny. Meleana Hinchman and John Parker have been instrumental in matters related to virology. Peter Schweitzer and his team at the Cornell Genomics Center have been a tremendous resource in helping me develop sequencing related technologies over the past four years. I thank the wonderful people who were part of my tenure as a graduate resident fellow at Hans Bethe House, in particular Karen and John Smeda, Erica Ostermann, Scott MacDonald, Julia Thom-Levy, Elizabeth Feeney, Xine Yao, Elizabeth Wayne, Nancy and Charlie Trautmann, and David Miller. They helped me build a home in Ithaca, for which I will always be thankful. My undergraduate mentor Dr. Georgia C. Papaefthymiou was the first person who gave me the opportunity to perform research. She has championed my work since 2011, and I am fortunate to have had her mentorship. I have been blessed with an amazing and supportive committee of physicists to guide my doctoral studies. Michelle Wang helped me tremendously to secure funding as a first year student, allowing me the freedom to pursue my areas of interest. Itai Cohen has shown me the importance of, and art to, scientific communication. Chris Myers has asked great questions of my work, which formed the second half of my doctorate and opened up new avenues to study viral infections in single cells. There are many others. viii TABLE OF CONTENTS BIOGRAPHICAL SKETCH ........................................................................................................................ v ACKNOWLEDGMENTS .......................................................................................................................... vii LIST OF FIGURES ..................................................................................................................................... xi LIST OF TABLES ................................................................................................................................... xviii LIST OF ABBREVIATIONS .................................................................................................................... xix Introduction ................................................................................................................................................... 1 PART I: Cell-free DNA sequencing to monitor infection ............................................................................ 4 Chapter 1: Physiological and historical origins of cell-free DNA ............................................................ 5 Chapter 2: Single-stranded DNA library preparation uncovers the origin and diversity of ultrashort cell- free DNA in plasma ................................................................................................................................ 10 1.2.0 A single-stranded ligation strategy to enrich ultrashort cfDNA ......................................... 11 1.2.1 Mitochondrial cfDNA in plasma measured by digital PCR ................................................ 12 1.2.2 ssDNA library preparation and fragmentation profiles ....................................................... 14 1.2.3 Improved recovery of mitochondrial and microbial cfDNA ............................................... 16 1.2.4 Donor-specific cfDNA from the mitochondria and autosomes .......................................... 19 1.2.5 Methods and sampling cohort description .......................................................................... 22 1.2.6 Ultrashort cell-free DNA provides a new perspective of origin and pathology .................. 25 Chapter 3: Urinary cell-free DNA is a versatile analyte for monitoring infections of the urinary tract . 28 1.3.0 cfDNA sequencing to inform infections
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