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C Copyright 2013 Marcela Ewert Sarmiento c Copyright 2013 Marcela Ewert Sarmiento Microbial Challenges and Solutions to Inhabiting the Dynamic Architecture of Saline Ice Formations Marcela Ewert Sarmiento A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2013 Reading Committee: Jody W. Deming, Chair John A. Baross Rebecca Woodgate Program Authorized to Offer Degree: School of Oceanography and Astrobiology Program University of Washington Abstract Microbial Challenges and Solutions to Inhabiting the Dynamic Architecture of Saline Ice Formations Marcela Ewert Sarmiento Chair of the Supervisory Committee: Walters Endowed Professor Jody W. Deming Oceanography Sea ice contains a microscopic network of brine inclusions effectively colonized by organisms from the three major clades of life. The architecture of this brine channel network is dynamic, with surface area, brine volume fraction, and brine salinity changing with temper- ature. This dynamic architecture may have also played a role in the origin and early evolution of life (Chapter 1). Sea-ice microorganisms experience multiple stressors, including low temperature, high salinity and fluctuations in those parameters. This dissertation discusses two bacterial adaptations to these challenges: the production of extracellular polysaccharide substances (EPS) and the accumulation of compatible solutes. Two Arctic bacteria were used as model organisms; the psychrophilic Colwellia psychrerythraea strain 34H (Cp34H), which grows at a comparatively narrow range of salinities, and the psychro- tolerant Psychrobacter sp. strain 7E (P7E), which grows at a broad range of salinities. Chapter 2 presents experimental results evaluating the establishment of the sea-ice bacterial community by means of selective enrichment of EPS. Chapter 3 presents field measurements indicating that biological components of the sea-ice brines, including bacterial cells and EPS from mixed sources (algal and bacterial), are expelled onto the ice surface and wicked upwards into snow, experiencing different degrees of cell loss depending on environmental conditions. Analysis of seasonal (Winter and Spring) in situ temperature and brine salinity data indicated that fluctuation regimes were significantly more energetic on the snow surface than in the ice column (Chapter 4), with implications for the microbial sea-ice population. Laboratory experiments exposing model organisms to freezing under constant and fluctu- ating regimes showed higher susceptibility to fluctuations by the stenohaline Cp34H than for the euryhaline P7E, with P7E undergoing fragmentation during the course of the freezing regime. The presence of compatible solutes significantly reduced cell loss in Cp34H. A synthesis of the microbial solutions to the challenges imposed by the dynamic structure of sea ice is discussed in Chapter 5, and testable hypotheses for future research were identified. Supporting information and the implementation of a science education and outreach activity based on this work is presented in the Appendices. TABLE OF CONTENTS Page List of Figures . v List of Tables . viii Chapter 1: Introduction . 1 1.1 The role of interstellar ice in the origin of prebiotic molecules . 3 1.2 Ice and the origin of life: a bottom-up approach . 5 1.3 Ice and the origin of life: a top-down approach . 7 1.4 Conclusions . 12 1.5 Acknowledgments . 13 Bibliography . 16 Chapter 2: Selective retention in saline ice of extracellular polysaccharides pro- duced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H (published as Ewert and Deming, 2011) . 23 2.1 Introduction . 24 2.2 Methods . 29 2.3 Results and discussion . 31 2.4 Conclusions . 35 2.5 Acknowledgments . 36 Bibliography . 41 Chapter 3: Bacterial and extracellular polysaccharide content of brine-wetted snow over Arctic winter first-year sea ice (published as Ewert et al., 2013) . 47 3.1 Introduction . 48 3.2 Methods . 50 3.3 Results . 55 3.4 Discussion . 58 i 3.5 Conclusions . 64 Bibliography . 71 Chapter 4: Environmental fluctuations and the role of compatible solutes in the survival of sea-ice bacteria . 78 4.1 Introduction . 79 4.2 Methods . 83 4.3 Results . 90 4.4 Discussion . 94 4.5 Conclusions . 104 4.6 Acknowledgments . 105 Bibliography . 116 Chapter 5: Sea Ice Microorganisms: Environmental Constraints and Extracellular Responses (published as Ewert and Deming, 2013) . 123 5.1 Introduction . 124 5.2 Sea ice as a microbial environment . 126 5.3 Extracellular responses to sea-ice environmental constraints . 137 5.4 Prospectus for future research . 143 5.5 Acknowledgments . 144 Bibliography . 152 Appendix A: Extracellular polysaccharide substances (EPS) from Colwellia psychrerythraea strain 34H . 166 A.1 Introduction . 166 A.2 Methods . 167 A.3 Results and discussion . 169 Bibliography . 178 Appendix B: Selective retention in artificial sea ice of extracellular polysaccharides from arctic surface seawater, sea ice and sea-ice brine . 180 B.1 Introduction . 180 B.2 Methods . 180 B.3 Results and discussion . 182 ii B.4 Conclusions . 183 Bibliography . 185 Appendix C: Complementary measurements of saline snow (published as Support- ing Information to Ewert etal, 2013) . 186 Bibliography . 195 Appendix D: Cell loss induced by osmotic down-shock in an extremely halophilic bacterial culture enriched from Arctic frost flowers . 197 D.1 Methods . 198 D.2 Results and discussion . 200 D.3 Conclusions . 200 Bibliography . 203 Appendix E: Strategies for osmolarity protection in Arctic sea-ice bacterial isolates as predicted by genomic analysis of related species . 204 E.1 Introduction . 204 E.2 Methods . 205 E.3 Results and discussion . 206 E.4 Conclusions . 209 E.5 Acknowledgments . 210 Bibliography . 224 Appendix F: Development of a public education and outreach activity linking Earth's cryosphere and icy planets in the search for life elsewhere . 227 F.1 Introduction . 227 F.2 Methods . 227 F.3 Results . 228 F.4 Conclusions . 229 Bibliography . 230 Appendix G: Below zero: looking for microbes in the coldest places . 231 G.1 Objectives . 231 G.2 Theoretical framework . 232 iii G.3 The activity . 233 G.4 Instructions for building the activity . 235 G.5 Experiences at Pacific Science Center . 237 G.6 Acknowledgments . 239 Bibliography . 246 Appendix H: Bajo Cero; buscando microbios en los lugares m´asfr´ıos:construcci´on de una actividad l´udicapara la presentaci´onen museos de ciencias . 247 H.1 Objetivos . 247 H.2 Marco te´orico . 248 H.3 La actividad . 249 H.4 Instrucciones para la construcci´onde la actividad . 251 H.5 Experiencias en el Centro de Ciencias del Pac´ıfico(PSC) . 253 H.6 Agradecimientos . ..
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