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Metagenomic Insights Into Microbial Metabolisms of a Sulfur-Influenced bioRxiv preprint doi: https://doi.org/10.1101/2020.01.31.929786; this version posted March 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Metagenomic Insights into Microbial Metabolisms of a Sulfur- 2 Influenced Glacial Ecosystem 3 4 Running Title: 5 Metagenomics of a Sulfur-Influenced Glacial Ecosystem 6 7 8 Christopher B. Trivedia, Blake W. Stampsa, Graham E. Laub, Stephen E. Grasbyc, Alexis S. 9 Templetonb, John R. Speara,# 10 11 aDepartment of Civil and Environmental Engineering, Colorado School of Mines, Golden, CO, 12 80401 USA 13 bDepartment of Geological Sciences, University of Colorado Boulder, Boulder, CO, 80309 USA 14 cGeological Survey of Canada-Calgary, Calgary, AB, T2L2A7 Canada 15 #Corresponding author: John R. Spear, [email protected] 16 17 18 Current addresses: 19 Christopher B Trivedi – Interface Geochemistry, GFZ German Research Centre for Geosciences, Helmholtz Centre 20 Potsdam, Potsdam, Brandenburg 14473 Germany 21 Blake W Stamps – UES, Inc., Dayton, OH, 45432 USA 22 Graham E Lau – Blue Marble Space Institute of Science, Seattle, WA, 98154 USA 23 24 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.31.929786; this version posted March 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 25 Abstract 26 Biological sulfur cycling in polar, low-temperature ecosystems is an understudied 27 phenomenon in part due to difficulty of access and the ephemeral nature of such environments. 28 One such environment where sulfur cycling plays an important role in microbial metabolisms is 29 located at Borup Fiord Pass (BFP) in the Canadian High Arctic. Here, transient springs emerge 30 from the toe of a glacier creating a large proglacial aufeis (spring-derived ices) that are often 31 covered in bright yellow/white sulfur, sulfate, and carbonate mineral precipitates that are 32 accompanied by a strong odor of hydrogen sulfide. Metagenomic sequencing from multiple 33 sample types at sites across the BFP glacial system produced 31 highly complete metagenome 34 assembled genomes (MAGs) that were queried for sulfur-, nitrogen- and carbon- 35 cycling/metabolism genes. Sulfur cycling, especially within the Sox complex of enzymes, was 36 widespread across the isolated MAGs and taxonomically associated with the bacterial classes 37 Alpha-, Beta-, Gamma-, and Epsilon- Proteobacteria. While this does agree with previous 38 research from BFP implicating organisms within the Gamma- and Epsilon- Proteobacteria as the 39 primary classes responsible for sulfur oxidation, our new data suggests putative sulfur oxidation 40 by organisms within Alpha- and Beta- Proteobacterial classes which was not predicted. These 41 findings indicate that in a low-temperature, ephemeral sulfur-based environment such as this, 42 functional redundancy may be a key mechanism that microorganisms use to co-exist whenever 43 energy is limited and/or focused by redox chemistry. 44 45 Importance 46 Borup Fiord Pass is a unique environment characterized by a sulfur-enriched glacial 47 ecosystem, in the low-temperature environment of the Canadian High Arctic. This unique 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.31.929786; this version posted March 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 48 combination makes BFP one of the best analog sites for studying icy, sulfur-rich worlds outside 49 of our own, such as Europa and Mars. The site also allows investigation of sulfur-based 50 microbial metabolisms in cold environments here on Earth. Herein, we report whole genome 51 sequencing data that suggests sulfur cycling metabolisms at BFP are more widely used across 52 bacterial taxa than predicted. From our data, the metabolic capability of sulfur oxidation among 53 multiple community members appears likely due to functional redundancy within their genomes. 54 Functional redundancy, with respect to sulfur-oxidation at BFP, may indicate that this dynamic 55 ecosystem hosts microorganisms that are able to use multiple sulfur electron donors alongside 56 other important metabolic pathways, including those for carbon and nitrogen. 57 58 1 Introduction 59 Arctic and Antarctic ecosystems such as lakes (Jungblut et al., 2016), streams 60 (Niederberger et al., 2009; Andriuzzi et al., 2018), groundwater-derived ice (aufeis; Grasby et al., 61 2014; Hodgkins et al., 2004), and saturated sediments (Lamarche-Gagnon et al., 2015) provide 62 insight into geochemical cycling and microbial community dynamics in low temperature 63 environments. One such ecosystem in the Canadian High Arctic, Borup Fiord Pass (BFP), is 64 located on northern Ellesmere Island, Nunavut, Canada and contains a transient sulfidic spring 65 system discharging through glacial ice and forming supra and proglacial ice deposits (aufeis) as 66 well as cryogenic mineral precipitates (Figure 1; Grasby et al., 2003). 67 Borup Fiord Pass is a north-south trending valley through the Krieger mountains at 68 81°01’ N, 81°38’ W (Figure 1, inset). The spring system of interest is approximately 210-240 m 69 above sea level and occurs at the toe of two coalesced glaciers (Grasby et al., 2003). The spring 70 system is thought to be perennial in nature but discharges from different locations along the 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.31.929786; this version posted March 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 71 glacier from year to year (Grasby et al., 2003; Gleeson et al., 2010; Wright et al., 2013; Lau et 72 al., 2017). However, given lack of winter observations it is not confirmed that spring flow is 73 year-round or limited to the warmer spring and summer months. However, growth of large aufeis 74 formations through the dark season support continued discharge through the winter. A lateral 75 fault approximately 100 m south of the toe of the glacier has been implicated in playing a role in 76 the subsurface hydrology, in that this may be one of the areas where subsurface fluid flow is 77 focused to the surface (Grasby et al., 2003; Scheidegger, et al. 2012). Furthermore, organic 78 matter in shales along this fault may be a source of carbon for subsurface microbial processes 79 such as biological sulfate reduction (BSR; Lau et al., 2017). 80 Previous research at BFP has surveyed microbial activity, redox bioenergetics (Wright et 81 al., 2013), the biomineralization of elemental sulfur (S0; (Grasby et al., 2003; Gleeson et al., 82 2011; Lau et al., 2017), and the cryogenic carbonate vaterite (Grasby, 2003). Wright et al. (2013) 83 produced a metagenome in the context of geochemical data to constrain the bioenergetics of 84 microbial metabolism from a mound of elemental sulfur sampled at the site in 2012, and found 85 that at least in surface mineral deposits, sulfur oxidation was likely the dominant metabolism 86 present among Epsilonproteobacteria. An exhaustive 16S rRNA gene sequencing study 87 conducted on samples collected in 2014-2017 revealed an active and diverse assemblage of 88 autotrophic and heterotrophic microorganisms in melt pools, aufeis, spring fluid, and surface 89 mineral deposits that persist over multiple years, contributing to a basal community present in 90 the system regardless of site or material type (Trivedi et al., 2018). However, to date no work has 91 been attempted to fully understand and characterize the metabolic capability of the microbial 92 communities adapted to this glacial ecosystem, including sulfur metabolism beyond the surface 93 precipitates at the site. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.31.929786; this version posted March 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 94 Microbial sulfur oxidation and reduction, which spans an eight electron transfer between 95 the most oxidized and reduced states, is important in a multitude of diverse extreme 96 environments, such as hydrothermal vents & deep subsurface sediments (Dahl and Friedrich, 97 2008), microbial mats (Ley et al., 2006; Feazel et al., 2008; Robertson et al., 2009), sea ice 98 (Boetius et al., 2015), glacial environments (Mikucki and Priscu, 2007; Purcell et al., 2014), and 99 Arctic hypersaline springs (Perreault et al., 2008; Niederberger et al., 2009). Two predominant 100 forms of sulfur-utilizing microorganisms exist: sulfur-oxidizing microorganisms (SOMs), which 0 101 use reduced compounds (e.g. H2S and S ) as electron donors, and sulfate-reducing 2- 2- 102 microorganisms (SRMs), which use oxidized forms of sulfur (e.g. SO4 and SO3 ) as electron 103 acceptors. SOMs are metabolically and phylogenetically diverse (Friedrich et al., 2001, 2005; 104 Dahl and Friedrich, 2008), and can often autotrophically fix carbon dioxide (CO2) while using a 105 variety of electron acceptors (Mattes et al., 2013). Likewise, SRMs can utilize a range of electron 106 donors, including organic carbon, inorganic carbon, methane, hydrogen, metallic iron (Enning et 107 al., 2012), and even heavier metals such as uranium, where the soluble U(VI) is converted to the 108 insoluble U(IV) under anoxic conditions (Spear et al., 1999, 2000). SRMs are particularly 109 important in sulfate-rich marine environments where they contribute as much as 50% of total 110 global organic carbon oxidation (Thullner et al., 2009; Bowles et al., 2014). 111 Some research has been conducted on microbial sulfur-cycling in low-temperature polar 112 environments in both Antarctica (Mikucki et al., 2009, 2016) and the Arctic (Niederberger et al., 113 2009; Purcell et al., 2014), including BFP (Gleeson et al., 2011; Grasby et al., 2012; Wright et 114 al., 2013).
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