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© Copyright 2020 Gordon Maxwell Showalter © Copyright 2020 Gordon Maxwell Showalter Acquisition, degradation, and cycling of organic matter within sea-ice brines by bacteria and their viruses Gordon Maxwell Showalter A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2020 Reading Committee: Jody W. Deming, Chair John A. Baross Jodi N. Young Program Authorized to Offer Degree: School of Oceanography University of Washington Abstract Acquisition, degradation, and cycling of organic matter within sea-ice brines by bacteria and their viruses Gordon Maxwell Showalter Chair of the Supervisory Committee: Prof. Jody W. Deming School of Oceanography Marine dissolved organic carbon (DOC) is a major component of the global carbon pool, and thus can have significant effects on global carbon cycling. Within the oceans, DOC is largely regulated by microbial communities, which can serve as both a source and sink of organic carbon. Microbial controls on DOC cycling within sea ice are especially relevant to global processes, as sea ice can act as an inhibitor of exchange between the ocean and the atmosphere while also affecting carbon export to the deep sea. However, how sea-ice communities influence DOC cycling, especially in very cold conditions of winter sea ice, is poorly understood. This dissertation explores how bacterial communities, which dominate winter sea ice, may influence DOC cycling. Chapter 1 presents an introduction of sea-ice microbial communities in the low-temperature, high salinity conditions which characterize sea-ice brines. How bacteria within brines swim in response to temperature, salinity, and chemical gradients in sea ice is presented in Chapter 2, which demonstrates a low-temperature record for directed bacterial swimming and suggests explanations for how bacteria position themselves within brines to access DOC. However, most DOC within the marine environment is too large for bacterial uptake, necessitating degradation by enzymes. Chapter 3 demonstrates bacterial extracellular enzyme activity both in a laboratory setting and in situ, showing growth-dependent enzyme activity down to –8˚C and up to 142 ppt salts and across a freeze-thaw cycle within sea ice and sea-surface microlayer samples. Finally, Chapter 4 presents a model of bacterially and virally mediated DOC cycling. This model uses simple differential equations, explained further in Appendix 1, to probe the potential existence of a viral shunt within sea-ice brines by demonstrating the role of bacteriophage in population dynamics of a theoretical brine, suggesting low viral production, high host-specificity, and virally-driven DOC cycling may be common within this environment. The results of this dissertation have implications for the understanding of DOC within polar seas and demonstrate the potential for active DOC cycling mediated by bacteria and their viruses within winter sea ice, which serves as an analog for very cold ice elsewhere. TABLE OF CONTENTS List of Figures ................................................................................................................................ iv List of Tables ................................................................................................................................. ix Chapter 1. An introduction to sea-ice carbon dynamics ........................................................... 12 1.1 The ocean as a carbon pool ........................................................................................ 12 1.2 Sea-ice communities .................................................................................................... 13 1.3 Sea ice and astrobiology ............................................................................................. 15 1.4 Sea ice across scales .................................................................................................... 16 Chapter 2. Low-temperature chemotaxis, halotaxis and chemohalotaxis by the psychrophilic marine bacterium Colwellia psychrerythraea 34H ................................................................... 21 2.1 Introduction ................................................................................................................. 22 2.2 Materials and methods ............................................................................................... 27 2.2.1 Bacterial cultures ...................................................................................................... 27 2.2.2 Experimental set-up and treatments .......................................................................... 28 2.3 Results and discussion ................................................................................................ 31 2.3.1 Chemotaxis, when Cp34H was grown at 8°C ........................................................... 31 2.3.2 Chemotaxis, when Cp34H was grown at –1°C ......................................................... 33 2.3.3 Halotaxis and chemohalotaxis .................................................................................. 34 2.3.4 Implications for microbial life within sea ice ........................................................... 37 i Chapter 3. Extracellular enzyme activity in hypersaline, low-temperature conditions by Colwellia psychrerythraea strain 34H and Psychrobacter sp. strain 7E and in Arctic sea ice and surroundings ........................................................................................................................ 53 3.1 Introduction ................................................................................................................. 54 3.2 Materials and methods ............................................................................................... 56 3.2.1 Cultured bacterial growth and harvest ...................................................................... 56 3.2.2 Laboratory enzyme activity assays ........................................................................... 58 3.2.3 Field experiments ...................................................................................................... 59 3.2.4 Rate calculation ......................................................................................................... 61 3.2.5 Bacterial counts ......................................................................................................... 61 3.3 Results .......................................................................................................................... 62 3.3.1 EEA of Cp34H and P7E grown at optimal conditions ............................................. 62 3.3.2 EEA of Cp34H grown at non-optimal conditions ..................................................... 63 3.3.3 EEA in environmental samples ................................................................................. 63 3.4 Discussion .................................................................................................................... 64 3.4.1 Patterns of activity suggesting psychrophilic nature ................................................ 66 3.4.2 EEA at the seawater/sea-ice interface ....................................................................... 69 3.4.3 Environmental implications ...................................................................................... 71 Chapter 4. Modeled viral dynamics: potential controls on infection and production rates within sea-ice brines .................................................................................................................... 87 4.1 Introduction ................................................................................................................. 88 4.2 Materials and methods ............................................................................................... 91 ii 4.2.1 Model framework ...................................................................................................... 91 4.2.2 Model analysis .......................................................................................................... 92 4.2.3 Model assumptions and simplifications .................................................................... 94 4.3 Results and discussion ................................................................................................ 95 4.3.1 Steady-state solution and Sobol’ analysis ................................................................. 96 4.3.2 Parameter estimation and tuning ............................................................................... 97 4.3.3 Lytic fraction estimate ............................................................................................ 101 4.3.4 DOC recycling ........................................................................................................ 102 4.3.5 Multispecies interactions ........................................................................................ 104 4.4 Conclusions ................................................................................................................ 107 Appendix 1. Equations of virus-bacteria population model ................................................. 130 Appendix 2. Cryopeg brines as a sub-zero, hypersaline environment comparison: Extracellular enzyme activity measurements........................................................................ 133 Appendix 3. Climate change and public health: A brief review of Canadian policies in Inuit Nunangat..................................................................................................................................
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