Relationship between dissolved organic matter quality and microbial community Authors: H. J. Smith, M. Dieser, D. M. McKnight, M. D. SanClements, and Christine M. Foreman, This is a pre-copyedited, author-produced PDF of an article accepted for publication in FEMS Microbiology Ecology following peer review. The version of record is available online at: https:// doi.org/10.1093/femsec/fiy090. Smith HJ, M Dieser, DM McKnight, MD SanClements, CM Foreman, “Relationship between dissolved organic matter quality and microbial community composition across polar glacial environments,” FEMS Microbiology Ecology, July 2018; 94(7):1-10. doi: 10.1016/ j.cmi.2018.01.003 Made available through Montana State University’s ScholarWorks scholarworks.montana.edu RESEARCH ARTICLE Relationship between dissolved organic matter quality and microbial community composition across polar glacial environments H.J. Smith1, M. Dieser1,2, D.M. McKnight3, M.D. SanClements3,4 and C.M. Foreman1,2,*,† 1Center for Biofilm Engineering, Montana State University, Bozeman, MT 59717, USA., 2Department of Chemical and Biological Engineering, Montana State University, Bozeman, MT 59717, USA., 3INSTAAR, University of Colorado Boulder, Boulder, CO 80303, USA. and 4National Ecological Observatory Network, Boulder, CO 80301, USA. ∗Corresponding author: Center for Biofilm Engineering, Montana State University, 311 Barnard Hall, Bozeman, MT 59717, USA. Tel: +406-994-7361; E-mail: [email protected] One sentence summary: Our results demonstrate the establishment of distinct microbial communities within ephemeral glacial meltwater habitats, with DOM-microbe interactions playing an integral role in shaping communities on local and polar spatial scales. Editor: Marek Stibal †Christine Foreman, http://orcid.org/0000-0003-0230-4692 ABSTRACT Vast expanses of Earth’s surface are covered by ice, with microorganisms in these systems affecting local and global biogeochemical cycles. We examined microbial assemblages from habitats fed by glacial meltwater within the McMurdo Dry Valleys, Antarctica and on the west Greenland Ice Sheet (GrIS), evaluating potential physicochemical factors explaining trends in community structure. Microbial assemblages present in the different Antarctic dry valley habitats were dominated by Sphingobacteria and Flavobacteria, while Gammaproteobacteria and Sphingobacteria prevailed in west GrIS supraglacial environments. Microbial assemblages clustered by location (Canada Glacier, Cotton Glacier and west GrIS) and were separated by habitat type (i.e. ice, cryoconite holes, supraglacial lakes, sediment and stream water). Community dissimilarities were strongly correlated with dissolved organic matter (DOM) quality. Microbial meltwater assemblages were most closely associated with different protein-like components of the DOM pool. Microbes in environments with mineral particles (i.e. stream sediments and cryoconite holes) were linked to DOM containing more humic-like fluorescence. Our results demonstrate the establishment of distinct microbial communities within ephemeral glacial meltwater habitats, with DOM-microbe interactions playing an integral role in shaping communities on local and polar spatial scales. Keywords: Biodiversity; Antarctica; Greenland; microbial; dissolved organic matter INTRODUCTION cycles. These icy environments are subject to relatively simi- lar environmental conditions, including low temperature, fre- Glaciers and ice sheets represent a distinct biome, dominated quent freeze-thaw cycles, seasonally low water availability, des- by diverse and biologically active microorganisms (Anesio and iccation and nutrient limitation, but vary in the degree of sur- Laybourn-Parry 2012; Boetius et al. 2015; Anesio et al. 2017), face melt and geochemical composition. As such, the presence that play a pivotal role in regional and global biogeochemical of distinct microbial communities in environmentally similar glacial meltwater habitats (Cameron et al. 2012, 2015, 2016; Stibal et al. 2015; Lutz et al. 2016; Uetake et al. 2016) offers intriguing questions about the factors influencing trends in community structure and function and the impacts of microorganisms on geochemical processes. While regional differences across glacial meltwater communities have been frequently attributed to local aeolian deposition, catchment geology, and physical and geo- graphical variables (Cameron et al. 2015, 2016; Cook et al. 2015; Musilova et al. 2015; Stibal et al. 2015; Lutz et al. 2016), these fac- tors may, indeed, have only a limited effect on community com- position. Findings from a growing number of investigations favor the development of habitat-specific ice surface communities, particularly those adapted to specific ecological niches (Mueller and Pollard 2004;Edwardset al. 2013; Musilova et al. 2015;Gawor et al. 2016; Franzetti et al. 2017). Dissolved organic matter (DOM) on ice sheets originates from a variety of allochthonous (i.e. terrestrial, marine or black car- bon) and autochthonous (i.e. in situ production) sources (Stibal et al. 2010; Stubbins et al. 2012;Legrandet al. 2013; Antony et al. 2014; Hood et al. 2015;Smithet al. 2017), both of which have been shown to vary in reactivity and may be highly bioavail- able to resident microbial communities (Hood et al. 2009; Antony et al. 2017;Smithet al. 2017). Many studies have targeted DOM dynamics on the surface of ice sheets (Anesio et al. 2009; Hod- Figure 1. Sampling locations in (A) the western margin of the Greenland Ice Sheet son et al. 2010; Cook et al. 2012 ; Stibal et al. 2012; Hood et al. 2015), and (B) the McMurdo Dry Valleys, Antarctica. and both deposition and in situ production have been linked to the biogeochemical evolution of DOM in supraglacial waters parameters, including major ions, nutrients, DOC concentra- (Hood et al. 2009; Stubbins et al. 2012; Telling et al. 2012; Antony tion, and fluorescing DOM characteristics were evaluated to infer et al. 2014; Musilova et al. 2017;Smithet al. 2017). Rather than their influence on microbial community composition. The pri- being passive receivers of allochthonous DOM, recent studies mary objective of this study was to link trends in bacterial bio- indicate that there are tight interactions between DOM produc- diversity to DOM quality across glacial systems, thus enabling tion and composition within bacterial communities in glacial better predictions regarding their function in the context of a surface habitats (Smith et al. 2016, 2017; Musilova et al. 2017). changing environment. Additionally, changes in microbial community structure have been correlated with dissolved organic carbon (DOC) concen- trations and the presence of distinct algal populations in Arc- METHODS tic snow and on glaciers, further attesting to the importance Field site description of interactions between organic carbon and microbial commu- nities (Lutz et al. 2016, 2017). In fact, major components of Sampling was conducted in the McMurdo Dry Valleys, Antarc- glacial carbon dynamics are functionally linked to trophic inter- tica and at the western margin of the GrIS (Fig. 1). The McMurdo actions between photo- and heterotrophs during algal blooms, Dry Valleys of Antarctica comprise the largest ice-free area of and within cryoconite granules and biofilms (Edward et al. 2011; the Antarctic continent and are classified as polar deserts with Takeuchi et al. 2014; Anesio et al. 2017; Lutz et al. 2017; Musilova <10 cm of precipitation per year. Mean annual temperatures et al. 2017;Smithet al. 2017). However, the mechanism by which range between −15◦Cand−30◦C. This barren region experiences the composition of DOM influences bacterial utilization and ulti- katabatic winds originating in the continental interior, which mately community composition is largely unknown. are important in controlling local climate, physical weathering Globally, glacial meltwater habitats are dominated by and material transport. Contrary to expectation, contributions cyanobacteria, Proteobacteria, Actinobacteria, Bacteriodetes, Aci- by marine aerosols are minor (Bottos et al. 2014; Bowman and dobacteria, Chloroflexi and Planctomycetes, with regional differ- Deming 2017). The two Antarctic sampling sites were comprised ences at lower levels of taxonomic resolution (Boetius et al. of glacially fed Antarctic stream ecosystems ∼70 km apart: (i) 2015). Given the habitat-specific selective pressures of cryo- The Cotton Glacier (CG) supraglacial stream (77◦07’S, 161◦40’E) environments, we hypothesize that bacterial assemblages are is ∼16 km long, consisting of a network of braided channels cut shaped by geochemistry, which provides the available energy through the ice, ultimately terminating into McMurdo Sound. sources necessary to support life. To test this scenario, glacial The CG stream receives a large amount of sedimentary deposits meltwater habitats from the Earth’s polar regions were inves- of unknown origin (fluvial, glacial or aeolian) from surround- tigated. Meltwater samples were collected from two glaciers in ing areas (Foreman et al. 2013). Sediments are primarily located the McMurdo Dry Valleys, Antarctica, (stream water, stream sed- on the lateral margins of the stream, and herein referred to as iments, glacial ice, snow, and cryoconite holes) and from the parafluvial sediments. CG stream water (n = 10), parafluvial sed- western margin of the Greenland Ice Sheet (GrIS) (supraglacial iments (n = 11), snow (n = 1) and surrounding ice (n = 5) were lakes and cryoconite holes). Illumina MiSeq 16S