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THE MICROBIOLOGY OF THE SULFUR-DOMINATED GLACIAL ECOSYSTEM AT BORUP FIORD PASS, AND HIGH ARCTIC LOW-TEMPERATURE SPRING ASSOCIATED MICROBIAL MATS by Christopher Bhartendu Trivedi A thesis submitted to the Faculty and Board of Trustees of the Colorado School of Mines in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Civil and Environmental Engineering). Golden, Colorado Date _____________________ Signed: _____________________ Christopher Bhartendu Trivedi Signed: _____________________ Dr. John R. Spear Thesis Advisor Golden, Colorado Date _____________________ Signed: _____________________ Dr. Terri S. Hogue Professor and Department Head Department of Civil and Environmental Engineering ii ABSTRACT Borup Fiord Pass (BFP) located on Ellesmere Island in the Canadian High Arctic is a unique low-temperature environment. BFP is a sulfur-dominated ecosystem that occurs within the Krieger mountains. Here, a subglacial spring emergences from the toe of a coalescence glacier. The presence of high concentrations of sulfur and low temperatures make BFP an excellent terrestrial analog for the study of potential astrobiological targets. High concentrations of sulfur also make BFP an ideal location for studying how microbial organisms can utilize reduced and oxidized forms of sulfur to thrive in cold environments. Yet, due to human influence Arctic research sites may not remain cold perpetually also making the location ideal to study climate change. Over field campaigns in 2014, 2016, and 2017, numerous samples were collected and analyzed for microbial community composition (16S rRNA gene sequencing), function (metagenomic sequencing), and aqueous geochemistry. 16S rRNA gene sequencing data revealed Flavobacterium was common to almost all samples. Sulfur-oxidizing microorganisms (Sulfurimonas, Sulfurovum, and Sulfuricurvum), and an organism that specializes in the disproportionation of inorganic sulfur compounds (Desulfocapsa) were also abundant in samples with high concentrations of sulfur compounds. To link the identified microbial taxa to function, assembly and binning of metagenomic sequence data was carried out and produced 31 reportable metagenome assembled genomes (MAGs), which revealed that sulfur oxidation may be a cosmopolitan process at BFP. Overall, results suggest that while sulfur cycling organisms dominate during acute events, a basal community structure appears to dominate over time and site type and that functional redundancy may be a key mechanism utilized by microorganisms for energy generation in this low-temperature environment. Finally, to address the changing Arctic climate the community composition and function of microbial iii mats found across Ellesmere Island was characterized. To my knowledge these are the most northern microbial mats ever identified, potentially acting as a barometer to study climate change and its effect on polar environments. Microbial community composition varied significantly between sample sites. Metagenomes were sequenced from one site, Ice River, revealing the potential for sulfur oxidation, nitrate/nitrite reduction, and carbon fixation via the reductive acetyl-CoA and reverse TCA cycles. Also found were genes that allow microorganisms to adapt to adverse conditions in extreme environments. High Arctic microbial communities help to guide our search for potential life on extraterrestrial worlds, and further enhance our knowledge of low-temperature ecosystems on Earth as our climate continues to change. iv TABLE OF CONTENTS ABSTRACT ….. ............................................................................................................................ iii LIST OF FIGURES ....................................................................................................................... ix LIST OF TABLES ......................................................................................................................... xi LIST OF ABBREVIATIONS ....................................................................................................... xii ACKNOWLEDGEMENTS ......................................................................................................... xiii CHAPTER 1 INTRODUCTION ............................................................................................... 1 1.1 Sulfur Metabolism in the High Arctic .................................................................................. 1 1.2 Permafrost hydrology and transient springs ......................................................................... 6 1.3 Challenges of studying microbiology at 81° N 81° W ......................................................... 8 1.4 Evolution of DNA Sequencing Technologies in Cryomicrobiology .................................... 9 1.5 Research objectives ............................................................................................................. 11 1.6 Conclusions ......................................................................................................................... 15 1.7 Publications associated with CSM graduate degree ........................................................... 15 1.8 References ........................................................................................................................... 16 CHAPTER 2 LOW-TEMPERATURE SULFIDIC-ICE MICROBIAL COMMUNITIES, BORUP FIORD PASS, CANADIAN HIGH ARCTIC ..................................... 22 2.1. Introduction ........................................................................................................................ 23 2.1.1 BFP Site Background ................................................................................................... 25 2.2 Materials and Methods ........................................................................................................ 26 2.2.1 Field Work and Sample Collection .............................................................................. 26 2.2.2 DNA Extraction and 16S rRNA Gene Library Sequencing ........................................ 30 2.2.3 Aqueous Geochemistry ................................................................................................ 32 v 2.3 Results ................................................................................................................................. 34 2.3.1 General Field Observations .......................................................................................... 34 2.3.2 Estimated Biomass and Sample QC............................................................................. 35 2.3.3 Melt Pools and 2016 Spring Fluid Samples ................................................................. 35 2.3.4 Aufeis Samples ............................................................................................................ 39 2.3.5 Mineral Precipitate Samples ........................................................................................ 41 2.3.6 Glacier Samples ........................................................................................................... 44 2.3.7 Additional Aqueous Geochemistry .............................................................................. 46 2.4 Discussion ........................................................................................................................... 47 2.5 Conclusion .......................................................................................................................... 56 2.6 Data Availability ................................................................................................................. 57 2.7 Acknowledgements ............................................................................................................. 57 2.8 References ........................................................................................................................... 58 CHAPTER 3 METAGENOMIC INSIGHTS INTO MICROBIAL METABOLISMS OF A SULFUR-DOMINATED GLACIAL ECOSYSTEM .................................. 64 3.1 Introduction ......................................................................................................................... 65 3.2 Results ................................................................................................................................. 70 3.2.1 Whole shotgun sequencing and assembly .................................................................... 70 3.2.2 Binning, MAG determination, and putative taxonomic identification ........................ 70 3.2.3 MAG recruitment by sample........................................................................................ 72 3.2.4 Sulfur cycling genes ..................................................................................................... 73 3.2.5 Carbon metabolism genes ............................................................................................ 77 3.2.6 Nitrogen cycling genes................................................................................................. 79 3.2.7 Hydrogen, Oxygen, and Hopanoids ............................................................................. 79 vi 3.3 Discussion ........................................................................................................................... 80 3.4 Conclusion .......................................................................................................................... 87 3.5 Methods .............................................................................................................................
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