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Gokul Jarishma Keriuscia Vol1 SUPRAGLACIAL SYSTEMS BIOLOGY OF DYNAMIC ARCTIC MICROBIAL ECOSYSTEMS A thesis submitted for the degree of Philosophiae Doctor (Doctor of Philosophy) by Jarishma Keriuscia Gokul (MSc, BTech (Hons), BSc) Interdisciplinary Centre for Environmental Microbiology Institute for Biological, Environmental and Rural Sciences Aberystwyth University May 2017 DECLARATION Word count of thesis: .……………………………………………………………………………….…………….57 348 DECLARATION This work has not previously been accepted in substance for any degree and is not being concurrently submitted in candidature for any degree. Candidate name ……………………………………………………………………………………………………….Jarishma Keriuscia Gokul Signature …………………………………………………………………………………………………………………. Date ………………………………………………………………………………………………………………………….30 May 2017 STATEMENT 1 This thesis is the result of my own investigations, except where otherwise stated. Where correction services have been used, the extent and nature of the correction is clearly marked in a footnote(s). Other sources are acknowledged by footnotes giving explicit references. A bibliography is appended. Signature …………………………………………………………………………………………………………………. Date ………………………………………………………………………………………………………………………….30 May 2017 STATEMENT 2 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signature …………………………………………………………………………………………………………………. Date ………………………………………………………………………………………………………………………….30 May 2017 i SUMMARY Arctic glacier surfaces are a biologically active region of the cryosphere, supporting several cosmopolitan microbial taxa. Bacterial communities across the different ice surfaces are spatially variable and significantly influenced by biogeography and biogeochemistry. In summer, the supraglacial surface reveals extensive cryoconite hole coverage that is correlated to surface albedo, melt rate, mass balance and biological activity. However, the relative importance of temporal changes on bacterial community composition and activity in these supraglacial niches have yet to be determined. To enhance this knowledge, community dynamics of bacteria in cryoconite, snow and meltwater streams were investigated synthetically and on Foxfonna ice cap, Foxfonna valley glacier and the Greenland Ice Sheet. By means of microscopy, metabolomics and high throughput sequencing of 16S rRNA genes and cDNA from 16S rRNA, the summer bacterial community was evaluated to determine the relative importance of taxa on supraglacial surfaces. This aided in unravelling the complex interactions that are prevalent in a simple microbial niche exposed to unique environmental conditions, nutritional deficits and geological constraints. Overall, the bacteria on Foxfonna and Greenland supraglacial surfaces display distinct seasonal transient behaviour. Taxa appear selective to their physical environment and biogeochemical state in the cryosphere, characterized by integral associations with the photoautotrophic Cyanobacteria, Phormidesmis priestleyi, that mediates formation of a robust microhabitat conglomerated with humics, extracellular polymeric substances and minerals that are essential to the diverse and productive cryoconite community. The rare biosphere provides a source for heterotrophic bacterial recruitment in cryoconite, snow and stream habitats, the latter of which exhibit high abundances of proteobacterial subclasses only minimally dissimilar from cryoconite during the boreal summer. Network analysis predicts that these taxa may be responsible for the observed seasonal shifts of activity in favourable conditions, while generating the essential nutrient reserves required during winter dormancy periods. ii ACKNOWLEDGEMENTS “Appreciation is a wonderful thing. It makes what is excellent in others belong to us as well.” ― Voltaire I would like to extend my sincere gratitude to my excellent supervisory team, Arwyn Edwards, Luis Mur and Tristram Irvine-Fynn, for their continued multifaceted assistance, support and guidance during four years of immensely enjoyable molecular and physical science as a member of the Cryosphere Microbiology Lab. Thank you to the South African National Research Fund (NRF), for awarding me a prestigious Study Abroad Scholarship, without which this work would not be possible. My thanks to Karen Cameron and Andy Hodson for assisting Arwyn and Tris with sample collection at field sites on the Greenland Ice Sheet and Foxfonna respectively. Additional thanks go to Gareth Griffith, Hilary Worgan, Dylan Gwynn-Jones, Alan Cookson, Luis Mur and Arwyn Edwards, for the use of their lab facilities, Kathleen Tailliart and Manfred Beckman for mass spectrometric processing, Joe Cook and Emma Wharfe for geochemistry processing, Eli Saetnan for support with co- occurrence networks, Matt Hegarty for performing Illumina sequencing, Nia Blackwell, Susan Girdwood, Toby Wilkinson and Andrew Detheridge for assistance with Ion Torrent sequencing and their priceless combined technical support. My appreciation goes to an ever-supportive cryosphere team: Sara Rassner for her invaluable research advice, PhD fellows Nia, Richard, Ottavia, André, Aaliyah, as well as research students Sean, Jeremy and Tom for maintaining an exuberant lab atmosphere during the largest scale of metabolomic preparation known to IBERS. I am grateful to Jenny, Dave, Brian, Tony and Jen, for welcoming me into their fold, especially Marta, Rose and Hannah for their continued support. Thank you to Abercoustic (formerly Aberystwyth Glee Club), particularly Georgia and Megan, and The University Singers, for helping me find my voice and the much- anticipated musical interludes. Special thanks to Kiri Kolt for her support and friendship through the ups and downs during these last few years and Graham Brand for teaching me to trust myself above all else. Finally, I would like to express my lifelong gratitude to my parents and sister for their never-ending support in the face of prosperity and adversity while guiding me to the next stepping stone in life, one that my 10-year-old self dreamt of: exploring and understanding how the universe and the organisms within it work together. Ubuntu. ― J.K.G. iii TABLE OF CONTENTS DECLARATION ........................................................................................................ i SUMMARY ............................................................................................................ ii ACKNOWLEDGEMENTS ....................................................................................... iii TABLE OF CONTENTS ........................................................................................... iv LIST OF FIGURES ................................................................................................... x LIST OF TABLES .................................................................................................. xvi LIST OF ABBREVIATIONS ................................................................................. xviii CHAPTER 1 - INTRODUCTION ...................................................................................... 1 1.1. THE SUPRAGLACIAL ECOSYSTEM OF GLACIERS AND ICE SHEETS ................. 3 1.1.1. The effect of aeolian distribution on ice surfaces ..................................... 4 1.1.2. Microbial ecology and diversity of ice sheets and glaciers........................ 5 1.1.2.1. Snow-derived habitats ........................................................................... 9 1.1.2.2. Sediment-rich habitats ......................................................................... 11 1.1.3. Specialisation of microbiota to supraglacial environments .................... 15 1.2. BIOGEOGRAPHIC, BIOTIC AND ABIOTIC EFFECTS ON SUPRAGLACIAL HABITATS ................................................................................................................ 17 1.3. IMPACT OF CLIMATE CHANGE ON POLAR SYSTEMS ................................... 19 1.4. SUPRAGLACIAL SYSTEMS BIOLOGY ............................................................. 20 1.5. THESIS AIMS AND OBJECTIVES .................................................................... 22 1.5.1. Central hypotheses .................................................................................. 22 1.5.2. Research aims and objectives .................................................................. 23 1.5.3. Thesis structure and experimental design............................................... 24 CHAPTER 2 - GENERAL METHODS ............................................................................. 25 2.1. LOCATION OF FIELD SITES ........................................................................... 25 2.2. SAMPLE COLLECTION AND PROCESSING..................................................... 26 2.2.1. Cryoconite sample collection................................................................... 26 2.2.2. Glacial water sample collection ............................................................... 28 2.3. METABOLOMICS .......................................................................................... 28 2.3.1. Metabolite extraction .............................................................................. 28 iv 2.3.2. Mass spectrometry and data processing ................................................. 29 2.4. NUCLEIC ACID EXTRACTION PROCESSES AND TREATMENT ........................ 30 2.4.1. Nucleic acid extraction from Foxfonna ice cap cryoconite...................... 31 2.4.2. Nucleic
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