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The Impact of Tiny Organisms: Microbial Communities and Disease States University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations 2016 The Impact of Tiny Organisms: Microbial Communities and Disease States Christel Sjöland Chehoud University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Microbiology Commons Recommended Citation Chehoud, Christel Sjöland, "The Impact of Tiny Organisms: Microbial Communities and Disease States" (2016). Publicly Accessible Penn Dissertations. 1645. https://repository.upenn.edu/edissertations/1645 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/1645 For more information, please contact [email protected]. The Impact of Tiny Organisms: Microbial Communities and Disease States Abstract In the last decade, primarily through the use of sequencing, much has been learned about the trillions of microorganisms that reside in human hosts. These microorganisms play a wide range of roles including helping our immune systems develop, digesting our food, and protecting us from the invasion of pathogenic organisms. My thesis focuses on the characterization of fungal, viral, and bacterial communities in humans, investigating the use of defined microbial communities to cure diseases in animal models, and examining the effects of human microbiome modifications through fecal microbiota transfers. In the first part of this thesis, I use deep sequencing of ribosomal RNA gene tags to characterize the composition of the bacterial, fungal, and archaeal microbiota in pediatric patients with Inflammatory Bowel Disease and healthy controls. Archaeal reads were rare in the pediatric samples, whereas an abundant amount of fungal reads was recovered. Pediatric IBD was found to be associated with reduced diversity in both fungal and bacterial gut microbiota, and specific Candida taxa were increased in abundance in the IBD samples. I, then, describe my use of a variety of experimental and computational methods to study the viral communities of immune-compromised lung transplant recipients. Anelloviruses, circular, single-stranded DNA viruses, were found in all lung samples but were 56 times more abundant in samples from lung transplant recipients as compared to healthy controls or HIV+ subjects. In the third part of this thesis, I describe the use of defined microbial communities in mice, and its ability to reduce the production of ammonia long term and mitigate hepatic encephalopathy. This was shown to be true in both mice on a normal protein diet or a low protein diet. Last, I investigate the transfer of viral communities between humans through FMT and characterize features associated with efficient ansmission.tr A case series where feces from a single donor were used to treat three children with ulcerative colitis was used for the analysis. Ultimately this work showed that multiple viral lineages do transfer between human individuals through fecal microbiota transplants, but in this case series none of the viruses were known to infect human cells. In this thesis, I elucidate numerous roles for the microbiome in pediatric patients with IBD and lung-transplant recipients, show exciting new finding about engineering the microbiota to help with hyperammonia, and finally investigate a possible limitation about using microbial communities as therapeutics. Together this body of work provides insights into the assemblage of tiny organisms that live within us, constantly contributing. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Cell & Molecular Biology First Advisor Frederic D. Bushman Second Advisor Gary D. Wu Subject Categories Microbiology This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/1645 THE IMPACT OF TINY ORGANISMS: MICROBIAL COMMUNITIES AND DISEASE STATES Christel Sjöland Chehoud A DISSERTATION in Cell and Molecular Biology Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2016 Supervisor of Dissertation Co-Supervisor of Dissertation _____________________________ _____________________________ Frederic D. Bushman, Ph.D. Gary D. Wu, M.D. Professor, Department of Microbiology Professor, Department of Gastroenterology Graduate Group Chairperson _____________________________ Daniel S. Kessler, PhD. Associate Professor of Cell and Developmental Biology Dissertation Committee Paul Bates, Ph.D., Professor, Department of Microbiology Ronald G. Collman, M.D., Professor, Department of Medicine Elizabeth Grice, Ph.D., Assistant Professor, Department of Dermatology Mark Goulian, Ph.D. Professor, Department of Biology THE IMPACT OF TINY ORGANISMS: MICROBIAL COMMUNITIES AND DISEASE STATES COPYRIGHT 2016 Christel Sjöland Chehoud This work is licensed under the Creative Commons Attribution- NonCommercial-ShareAlike 3.0 License To view a copy of this license, visit http://creativecommons.org/licenses/by-ny-sa/2.0/ DEDICATION To my family, my secret weapon. iii ACKNOWLEDGMENT I would like to extend my deepest gratitude to all those who supported me throughout my years in graduate school. I am grateful to my mentors, Rick Bushman and Gary Wu. Rick’s wisdom, kindness, and enthusiasm for all things related to science have been pivotal in my development as a scientist and as a person. Gary’s ability to find insight in any dataset has taught me the importance of thinking critically. Elizabeth Grice, my “third” advisor, has always eagerly provided encouragement and guidance. Paul Bates has supported me through my MVP years, always willing to share his endless knowledge on science-related matters. I am indebted to Ron Collman, Mark Goulian, Jim Lewis and Hognzhe Li for their feedback and advice, and to Sara Cherry for her rigorousness which helped me pass my prelims. This work would not have been possible without the supportive and collaborative environment of the Bushman Lab. I thank Aubrey Bailey, Kyle Bittinger, Erik Clarke, Serena Dollive, Anatoly Drygra, Nirav Malani, Sam Minot, Scott Sherrill-Mix, and Rohini Sinha for their computational insights. I am appreciative of Laurie Zimmerman and Arwa Abbas’s artistic talents. I am grateful to my wonderful baymates, Alexandra Bryson and Jacque Young. The analysis could not have been done without the efforts of the experimental technicians in our lab, Stephanie Grunberg, Chris Hoffmann, Young Hwang, Abby Lauder, Alice Laughlin, and Frances Male, and rotation students, Amy Davis, Elizabeth Loy, and Seth Zost. I am also thankful for invaluable insight and advice from Fabiana Hoffmann, Brendan Kelly, Chris Nobles, and Vesa Turkki. Members of the Wu lab, including Lindsey Albenberg, Lillian Chau, Elliot Friedman, Colleen Judge, Sue Keilbaugh, Josie Ni, David Shen and Sarah Smith, have taught me everything I know about gastroenterology and provided me with a rich source of collaboration. I would like to acknowledge members of Grice lab, Geoffrey Hannigan, Adam SanMiguel, and Amanda Tyldsley, who were there for me during my first rotation and remained my friends throughout graduate school. iv Emily Roberts prepared me for the immunology portion of my prelim and has been a great motivator in science and in life. I am grateful to my GCB friends, Eric Chen and Yuchao Jiang, and, particularly, Varun Aggarwala who has been a source of support and advice since the very beginning of my graduate school years. I am grateful to my Whitehall High School friends, Alex Beers, Hector Moreno, Kaitlin Reed, Liz Rice, and Jill Richards, teachers, Mr. Adams and Mr. Stout, and counselor, Ms. McGill. I am indebted to my Princeton mentors, David Botstein, Tullis Onstott, and Bess Ward, and Integrated Science friends. My Broad mentors, Shawna Young, Eboney Smith, Bruce Birren, Brian Haas, and Dirk Gevers, introduced me to the microbiome back in 2008 and sparked this 8 year adventure. I am additionally grateful to my colleagues at Second Genome, particularly Todd DeSantis, Janet Warrington and Justin Kuczynski. Finally, I am thankful for the unconditional love, encouragement and support of my family, both nearby and around the world in Brazil, Canada, Lebanon, Sweden, and Venezuela. My parents, Albert and Georgette, sister, Grace, and husband, Erik, have been my biggest blessing during my graduate years, and throughout my life. v ABSTRACT THE IMPACT OF TINY ORGANISMS: MICROBIAL COMMUNITIES AND DISEASE STATES Christel Sjöland Chehoud Frederic D. Bushman Gary D. Wu In the last decade, primarily through the use of sequencing, much has been learned about the trillions of microorganisms that reside in human hosts. These microorganisms play a wide range of roles including helping our immune systems develop, digesting our food, and protecting us from the invasion of pathogenic organisms. My thesis focuses on the characterization of fungal, viral, and bacterial communities in humans, investigating the use of defined microbial communities to cure diseases in animal models, and examining the effects of human microbiome modifications through fecal microbiota transfers. In the first part of this thesis, I use deep sequencing of ribosomal RNA gene tags to characterize the composition of the bacterial, fungal, and archaeal microbiota in pediatric patients with Inflammatory Bowel Disease and healthy controls. Archaeal reads were rare in the pediatric samples, whereas an abundant amount of fungal reads was recovered. Pediatric IBD was found to be associated with reduced diversity in both
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