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Bacterial Communities Associated with Chronic Rhinosinusitis and the Impact of Mucin

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Bacterial Communities Associated with Chronic Rhinosinusitis and the Impact of Mucin Bacterial communities associated with chronic rhinosinusitis and the impact of mucin degradation on Staphylococcus aureus physiology A DISSERTATION SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY Sarah Kathleen Lucas IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Advisor: Ryan C. Hunter August 2020 © Sarah Kathleen Lucas 2020 Acknowledgements First, this thesis was made possible by the support of the Microbiology, Immunology, and Cancer Biology graduate program, and the faculty and staff of the Department of Microbiology & Immunology at the University of Minnesota. The contribution of the research community and resources available to me at the University of Minnesota cannot be overstated, and I feel very fortunate to have had the opportunity to work within a community that upholds high scholarly standards and are also a pleasure to be around. I would like to extend my deepest gratitude to several individuals for their support during my doctoral training: My advisor, Dr. Ryan Hunter: Thank you for the confidence you had in me, especially in the times when I scarcely believed in myself. Thank you for your patience, and for being the first true mentor I ever had. My labmates: it was a pleasure to conduct research alongside you all. My daily sounding boards for far-out ideas, and encouragement to jump into experiments and just “see what happens”. The members of my thesis committee: Gary Dunny, Mark Herzberg, and Dan Knights. Thanks for all the great feedback in our meetings. Your comments on my work over the years have always been constructive. There would be times in our annual meetings where I would find great motivation in your enthusiasm of the data I presented. I hope I have absorbed some of your wisdom these past few years. Dylan White, Elise Breed, and Mark Daniel: thank you for your friendship and camaraderie over the years. Your willingness to grab a beer together at Stub and Herbs at the end of a long day made a world of difference. My family, Mom, Dad, Andrea, and Conrad: thank you for being a strong support system for me. For sharing in all the ups and downs that happen. For still reacting with shock every Minnesota winter when I convey the weekly weather report. Monica DiMuzio and Jessica Myers: You two are my rocks. My best friends since grade school. Thank you for your almost daily support. Our friendship has seen a lot of “education”. And last, but not least, my husband Dr. Christopher Fernandez: I am so fortunate to be married to someone I admire and love as much as you. Thank for being my home wherever our geographical home may be. i Table of Contents List of Tables .................................................................................................................... iv List of Figures .................................................................................................................... v Chapter 1: Introduction .................................................................................................. 1 Chronic rhinosinusitis: epidemiology, etiology, and treatment ...................................... 2 Bacteriology of Chronic Rhinosinusitis .......................................................................... 7 New hypotheses: Mucin-microbe interactions in CRS ................................................. 14 Chapter 2: 16S rRNA gene sequencing reveals site-specific signatures of the upper and lower airways of cystic fibrosis patients† .............................................................. 17 Summary ....................................................................................................................... 18 Introduction ................................................................................................................... 19 Materials and Methods .................................................................................................. 21 Results ........................................................................................................................... 24 Discussion ..................................................................................................................... 31 Acknowledgements ....................................................................................................... 34 Figures........................................................................................................................... 35 Chapter 3: The microbiome of chronic rhinosinusitis in a cystic fibrosis patient cohort at University of Minnesota ................................................................................. 40 Summary ....................................................................................................................... 41 Introduction ................................................................................................................... 42 Materials and Methods .................................................................................................. 44 Results ........................................................................................................................... 47 Discussion ..................................................................................................................... 50 Acknowledgements ....................................................................................................... 51 Tables ............................................................................................................................ 52 Figures........................................................................................................................... 55 ii Chapter 4: Anaerobic mucin degrading bacterial communities differentiate the microbiome in chronic rhinosinusitis and can impact physiology of nasal pathobiont Staphylococcus aureus ..................................................................................................... 59 Summary ....................................................................................................................... 60 Introduction ................................................................................................................... 62 Materials and Methods .................................................................................................. 65 Results ........................................................................................................................... 71 Discussion ..................................................................................................................... 80 Acknowledgements ....................................................................................................... 85 Tables ............................................................................................................................ 87 Figures........................................................................................................................... 92 Chapter 5: Conclusion ................................................................................................. 100 Summary of research .................................................................................................. 101 Future Directions ........................................................................................................ 104 Concluding Remarks ................................................................................................... 106 Bibliography .................................................................................................................. 109 Appendices ..................................................................................................................... 131 Appendix A: Supplementary Information for Chapter 2 - 16S rRNA gene sequencing reveals site-specific signatures of the upper and lower airways of cystic fibrosis patients † ..................................................................................................................... 132 Appendix B: Bioorthogonal non-canonical amino acid tagging reveals translationally active subpopulations of the cystic fibrosis lung microbiota† .................................... 143 iii List of Tables Table 3.1 CF-CRS patient clinical information ................................................................ 52 Table 3.2 Prevalence and abundance of ASVs of top 20 genera in CF-CRS samples ..... 53 Table 4.1 Demographic and clinical data for FESS patients ............................................ 87 Table 4.2 Prevalence and average relative abundance of anaerobe features* in CRS and non-CRS samples .............................................................................................................. 88 iv List of Figures Figure 2.1 Bacterial Load in Sinus and Lung Samples. .................................................... 35 Figure 2.2 Bacterial community composition of the upper and lower airways. ............... 36 Figure 2.3 Alpha diversity of CF maxillary sinuses differs from CF lung sputum. ......... 37 Figure 2.4 Ordination of weighted Unifrac distances. ...................................................... 38 Figure 2.5 BugBase analysis of PICRUSt-predicted metagenomes. ................................ 39 Figure 3.1 CF-CRS sinus communities differentiate by Proteobacteria or Firmicutes. ... 56 Figure 3.2 DPCoA of bacterial community composition with clinical factors................. 57 Figure 3.3. Shannon diversity and dominant
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