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Characterizing Early-Life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach

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Characterizing Early-Life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 5-2016 Characterizing Early-life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach Weili Xiong The University of Tennessee, Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Genetics and Genomics Commons, and the Systems Biology Commons Recommended Citation Xiong, Weili, "Characterizing Early-life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach. " PhD diss., University of Tennessee, 2016. https://trace.tennessee.edu/utk_graddiss/3672 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Weili Xiong entitled "Characterizing Early-life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Life Sciences. Robert L. Hettich, Major Professor We have read this dissertation and recommend its acceptance: Jeffrey M. Becker, Mircea Podar, Chongle Pan, Loren J. Hauser Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Characterizing Early-life Microbiome Functionality in Premature Infant Gut by a Metaproteomics Approach A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Weili Xiong May 2016 ACKNOWLEDGEMENTS I would like to express my deepest gratitude to the following people who have always supported and encouraged me in this Ph.D. journey. Without their patience, guidance and persistent help, this dissertation would not have been completed. First of all, I would like to thank my advisor Dr. Robert Hettich for his guidance, support and dedication to helping me complete this dissertation. In my graduate life, he was an excellent mentor who helped me develop expertise in all aspects of scientific research, and also a “father” who always display trust and encouragement that allowed me to grow whenever I got challenged. I am grateful for all things I have learnt from him, especially his enormous scientific enthusiasm and positive spirit, and all opportunities he has provided during my time working with him. I would like to thank my committee members: Dr. Jeffrey Becker, Dr. Mircea Podar, Dr. Chongle Pan and Dr. Loren Hauser for their effort and valuable comments in this dissertation. Their inspiration and knowledge helped me think from different perspectives and broaden the scope of my project. Their time and inputs to my dissertation are greatly appreciated. I would like to thank all my lab colleagues for their guidance, discussions and encouragement throughout my PhD life. Thank you for the time when we share joys and difficulties of being a graduate student. In particular, I would thank Dr. Richard Giannone and Dr. Paul Abraham for their substantial help in teaching me all technical aspects of mass spectrometry experiments and always providing support and suggestions whenever I need their help. I would also like to acknowledge and thank the Genome Science and Technology Program for providing me this great opportunity and environment to pursue my scientific career. ii This project allowed me to collaborate with Dr. Jillian Banfield from University of Berkeley and Dr. Michael Morowitz from University of Pittsburg whom I had fantastic experience working with and would like to thank for their contributions in this project. Lastly, I would like to thank my family and all my friends. I want to give great thanks to my parents, who made my education a priority and always supported and believed in me. I thank my beloved husband, Xi Wang, for giving me constant love, care, support and patience that helped me through difficult times and made it possible for me to complete my degree. iii ABSTRACT Microbes inhabit all parts of human body that are exposed to the environment and their interactions with human host mutually benefit each other and play significant roles in human health and diseases. The human gastrointestinal tract harbors the largest population of the microbiota and has gained broad research attention and efforts over the past decade. Colonization of the gut by microbes begins at birth and this early-life bacterial establishment can impact infants’ health and even the human health and lifestyle across an entire life span. Recent studies on community structure and composition of infant gut microbiota have revealed the species shifts and variations during early bacterial colonization of the infant gut. However, little is known about functional activities of the community and how these functions change in response to different life events. Therefore, comprehensive proteomic characterization of the infant gut microbiome is needed to elucidate biological activities in this complex ecosystem. In this dissertation, we first developed a metaproteomics pipeline integrating both experimental and informatics components with careful considerations to simultaneously access microbial and human host proteins contained in infant fecal samples. The developed approach was applied in a longitudinal study of a healthy premature infant gut, revealing the overall metabolic cooperation between the human host and the gut microbiota and the temporal functional shifts in both microbiome and corresponding host response during the colonization process. To further investigate the commonalities and differences of gut microbiome between individuals, time- series metaproteomic studies were performed in three more premature infants, uncovering common core proteins/metabolic pathways established during early life microbiome establishment, as well as unique pathways that were specific to particular infants or present in certain colonization time period. In a broad perspective, the approaches and results presented in iv this dissertation have provided insights into functions and activities of human gut ecosystem, and developed techniques and outlined general considerations that can be extended to proteome characterization of all complex ecosystems. v TABLE OF CONTENTS CHAPTER 1. Introduction to mass spectrometry based metaproteomic characterization of human gut microbiome................................................................................................................. 1 1.1 Meta-omics technologies enable microbial community functional characterization ............ 1 1.1.1 Microbial community ..................................................................................................... 1 1.1.2 Metaproteomics among various –omics technologies .................................................... 3 1.2 Mass spectrometry (MS) based proteomics and metaproteomics ......................................... 8 1.3 Metaproteomics of human gut microbiome ........................................................................ 12 1.3.1 Introduction to human microbiome .............................................................................. 12 1.3.2 Current human gut metaproteome studies .................................................................... 14 1.4 Scope of the dissertation ..................................................................................................... 23 CHAPTER 2. Experimental and computational platform for human gut microbiome research ........................................................................................................................................ 25 2.1 General workflow for metaproteome measurements of human gut microbiome ................ 25 2.2 Sample preparation .............................................................................................................. 27 2.2.1 Sample collection ......................................................................................................... 27 2.2.2 Direct versus indirect sample preparation method ....................................................... 28 2.2.3 Cell lysis and proteome extraction ............................................................................... 29 2.2.4 Protein digestion ........................................................................................................... 31 2.3 Liquid chromatography ....................................................................................................... 31 2.4 Mass spectrometry instrumentation .................................................................................... 35 2.4.1 Ionization sources ......................................................................................................... 35 2.4.2 Mass analyzer and detector ........................................................................................... 38 2.4.3 Data acquisition in mass spectrometry ......................................................................... 43 2.4.4 Tandem mass spectrometry .........................................................................................
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