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University of Florida Thesis Or Dissertation BIOPRECIPITATION: THE CONNECTION BETWEEN MICROBIOLOGY AND METEOROLOGY By RACHEL ELAINE JOYCE A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2020 © 2020 Rachel Joyce To Mom and Dad ACKNOWLEDGMENTS I want to first and foremost thank my advisor, Dr. Brent Christner, who has made this research possible. His mentorship and support gave me the confidence to carry out my dissertation research. Without a doubt, I would not be the scientist that I am today, with such an unwavering passion for scientific research, if I had not gotten the encouragement that I received from Dr. Christner, and for that I am incredibly grateful. I would also like to thank all of my committee members for agreeing to oversee my PhD and offering me guidance and advice: Dr. Bryan Kolaczkowski, Dr. Ana Conesa, and Dr. Corene Matyas. I want to acknowledge the friends who proved to be an incredible support system over the last six years: To James Ramsden, who has worked with me in the lab for over a year and is always willing to go above and beyond to get work done; To Christina Davis, who was my first friend and confidant at UF; and Rachel Moore, whose sheer excitement about bioaerosols and microbiology is enough to keep me going even on my worst days; To the ladies of LSU--Heather Lavender, Dr. Noelle Bryan, and Dr. Amanda Achberger—who even after four years of moving apart, are always there to offer me a shoulder to lean on; To my two biggest role models, my mom and dad, who showed me how far hard work and dedication can get you in life; To all three of my siblings, Alex, Chris, and Luke, because I love them more than anything; And to my rock, Christopher Wilson, who has kept me grounded and sane and smiling even through the toughest of times. This research was funded by The National Science Foundation (DEB-1241161 and -1643288). 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF TABLES ...........................................................................................................................8 LIST OF FIGURES .......................................................................................................................10 LIST OF OBJECTS .......................................................................................................................12 LIST OF ABBREVIATIONS ........................................................................................................13 ABSTRACT ...................................................................................................................................15 CHAPTER 1 INTRODUCTION ..................................................................................................................17 Ice Nucleation .........................................................................................................................17 The Physics of Water and Ice Nucleation .......................................................................17 Heterogeneous Ice Nucleation in the Troposphere .........................................................20 Discovery of Biological Ice Nucleation ..........................................................................24 Biological Ice Nucleation .......................................................................................................26 Characterization of the Bacterial Ice Nucleation Protein ................................................26 Ice Nucleation in Fungi, Lichens, Pollen, and Algae ......................................................31 Applications of Biological Ice Nucleation ......................................................................33 Aeromicrobiology ...................................................................................................................34 Airborne Microorganisms and Disease Transmission .....................................................34 Emissions of Airborne Microorganisms ..........................................................................38 Hight Altitude and Cloud Microbiology .........................................................................41 Potential Influence of Biological Ice Nuclei on Meteorology ................................................43 Biological INPs in Air, Cloud, and Precipitation Samples .............................................43 Challenges and Limitations to Studying Biological INPs ...............................................48 Use of Biological INPs in Numerical Cloud and Climate Models .........................................51 Purpose of This Research .......................................................................................................56 2 CHARACTERIZATION AND SOURCE IDENTIFICATION OF BIOLOGICAL ICE NUCLEATING PARTICLES DEPOSITED YEAR-ROUND IN SUBTROPICAL PRECIPITATION ...................................................................................................................60 Overview .................................................................................................................................60 Methods ..................................................................................................................................62 Precipitation Sampling ....................................................................................................62 Quantification of INPs and Cells .....................................................................................63 Amplification and Sequencing of 16S rRNA Genes .......................................................64 Inorganic and Organic Chemistry ...................................................................................66 5 Analysis of Meteorological Data and Ecoregions ...........................................................68 Statistical Analyses ..........................................................................................................72 Results.....................................................................................................................................73 Total, Biological, and Bacterial INPs in Louisiana Precipitation ...................................73 Exploratory Factor Analysis of the INP Data ..................................................................75 INP Factor Concentrations Correlate With the Physical, Chemical, and Microbiological Data ...................................................................................................76 INP Factors Correlate with Season, Cloud Type, and the Air Mass History ..................77 Correlations Between Abundances of Bacterial Operational Taxonomic Units and INPs..............................................................................................................................79 Discussion ...............................................................................................................................80 INP “Classes” Identified in Louisiana Precipitation .......................................................80 Potential Geographic Origins of INP Classes in Louisiana Precipitation .......................82 INP Concentration as a Function of Season and Meteorology ........................................84 Potential Phylogenetic and Geographic Sources of the Ice Nucleating Bacteria ............85 Potential Implications for Biological INPs on Meteorological Processes .......................87 Concluding Remarks ..............................................................................................................89 3 INDUCTION OF ICE NUCLEATION ACTIVITY IN NOVEL ICE+ BACTERIA ..........100 Overview ...............................................................................................................................100 Methods ................................................................................................................................102 Sample Collection .........................................................................................................102 Bacterial Culturing ........................................................................................................102 Immersion Freezing Assays for Ice Nucleation Activity ..............................................104 Nutrient Limitation Experiments ...................................................................................105 Identification of the Bacterial Isolates ...........................................................................106 Results...................................................................................................................................107 Primary Enrichments of Arid Topsoil and Sleet Samples .............................................107 Dependence of Ice Nucleation Activity on Culture Age ...............................................107 Induction of IN Activity in Isolates AZ_82Pink and AZ_82Red ..................................110 Characterization of the Bacterial INP in AZ_82Pink ....................................................112 Discussion .............................................................................................................................113 Concluding Remarks ............................................................................................................121 4 SIZE-RESOLVED BIOLOGICAL INPS IN NIMBOSTRATUS
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