Molecular and biogeochemical evidence for methane cycling beneath the western margin of the Greenland Ice Sheet

The ISME Journal (2014) 8, 2305–2316 & 2014 International Society for Microbial Ecology All rights reserved 1751-7362/14 www.nature.com/ismej ORIGINAL ARTICLE Molecular and biogeochemical evidence for methane cycling beneath the western margin of the Greenland Ice Sheet Markus Dieser1,5,6, Erik LJE Broemsen1,5, Karen A Cameron2,7, Gary M King1, Amanda Achberger1, Kyla Choquette3, Birgit Hagedorn3, Ron Sletten4, Karen Junge2 and Brent C Christner1 1 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA; 2Applied Physics Laboratory, Polar Science Center, University of Washington, Seattle, WA, USA; 3Applied Science Engineering and Technology Laboratory, Environment and Natural Resources Institute, University of Alaska Anchorage, Anchorage, AK, USA and 4Department of Earth and Space Sciences, University of Washington, Seattle, WA, USA Microbial processes that mineralize organic carbon and enhance solute production at the bed of polar ice sheets could be of a magnitude sufficient to affect global elemental cycles. To investigate the biogeochemistry of a polar subglacial microbial ecosystem, we analyzed water discharged during the summer of 2012 and 2013 from Russell Glacier, a land-terminating outlet glacier at the western margin of the Greenland Ice Sheet. The molecular data implied that the most abundant and active component of the subglacial microbial community at these marginal locations were bacteria within the order Methylococcales (59–100% of reverse transcribed (RT)-rRNA sequences). mRNA transcripts of the particulate methane monooxygenase (pmoA) from these taxa were also detected, confirming that methanotrophic bacteria were functional members of this subglacial ecosystem. Dissolved methane ranged between 2.7 and 83 lM in the subglacial waters analyzed, and the concentration was inversely correlated with dissolved oxygen while positively correlated with electrical conductivity. Subglacial microbial methane production was supported by d13C-CH4 values between  64% and  62% together with the recovery of RT-rRNA sequences that classified within the Methanosarcinales and Methanomicrobiales. Under aerobic conditions, 498% of the methane in the subglacial water was consumed over B30 days incubation at B4 1C and rates of methane oxidation were estimated at 0.32 lM per day. Our results support the occurrence of active methane cycling beneath this region of the Greenland Ice Sheet, where microbial communities poised in oxygenated subglacial drainage channels could serve as significant methane sinks. The ISME Journal (2014) 8, 2305–2316; doi:10.1038/ismej.2014.59; published online 17 April 2014 Subject Category: Geomicrobiology and microbial contributions to geochemical cycles Keywords: Greenland Ice Sheet; methane; methanogenesis; methanotrophy; subglacial aquatic environment Introduction Environments below inland portions of the Greenland Ice Sheet are dark, cold and poorly ventilated, with basal melt in regions of elevated heat flux Correspondence: BC Christner, Department of Biological Sciences, Louisiana State University, 202 Life Sciences Building, Baton Rouge, LA 70803, USA. E-mail: 5 These authors contributed equally to this work. 6 Current address: Center for Biofilm Engineering, Montana State University, 366 EPS Building, Bozeman, MT 59715, USA. 7 Current address: Department of Geochemistry, Geological Survey of Denmark and Greenland, Øster Voldgade 10, 1350 Copenhagen, Denmark. Received 26 December 2013; revised 8 March 2014; accepted 14 March 2014; published online 17 April 2014 providing the main source of liquid water at the bed (Bell, 2008). In the absence of direct exchange with the atmosphere, aerobic respiration and chemical oxygen consumption create anoxia, providing conditions favorable for obligately anaerobic processes such as methanogenesis (Skidmore et al., 2005, 2010; Tranter et al., 2005; Wadham et al., 2008). Whether or not the basal zones of ice sheets are sources of atmospheric methane will depend on the in situ rates of methane production and consumption (that is, methanotrophy) and how effectively gases are advected to the margin. Although it is hypothesized that substantial subglacial methane reservoirs exist (Wadham et al., 2012), the release of which could potentially influence atmospheric methane concentrations during deglaciation Methane cycling beneath the Greenland Ice Sheet M Dieser et al 2306 (Wadham et al., 2008, 2012), there have been few data available on microbial carbon transformations beneath ice sheets. Measurements of methane excesses in basal ice (Souchez et al., 1995; Miteva et al., 2009) and frozen water (Christner et al., 2012) have suggested that methanogenesis occurs beneath the Greenland Ice Sheet. It is also possible that the erosion of preglacial permafrost through glaciological processes could provide an additional source of legacy methane under the ice (Miteva et al., 2009). Measurements of methane production in laboratory microcosms and molecular analyses have confirmed that methanogenic archaea are active members of the microbial communities in these biomes (Boyd et al., 2010; Stibal et al., 2012a, b). However, data to assess carbon dynamics in these ecosystems have been challenging to obtain, and our understanding about the structure and diversity of microbial communities inhabiting the basal environments of polar ice sheets is still very limited. Here we present molecular and biogeochemical data from a study that investigated the role of microbes in subglacial carbon transformations in West Greenland. Near the ice sheet margin, surface melt enters the subglacial hydrological system through crevasses and moulins, transporting water, atmospheric gases, nutrients and allochthonous carbon to the base (Tranter et al., 2005). Microbiological and physicochemical characteristics of this aqueous environment were examined by collecting and analyzing subglacial outflows from the western margin of the Greenland Ice Sheet near Kangerlussuaq during the melt season in 2012 and 2013. Our results show the dominance of active methanotrophic bacteria as well as phylotypes related to a diverse assortment of obligately anaerobic bacteria and methanogenic archaea, confirming that a range of oxic to anoxic conditions are present in the subglacial environment at the marginal zone. The implications of unearthing a methanotrophic component in the subglacial ecosystem, and how effluxes and cycling of methane may occur beneath the Greenland Ice Sheet, are discussed. Materials and methods Study site description Sampling at the western margin of the Greenland Ice Sheet was conducted at Russell Glacier (67170 600 N, 501100 500 W), a land-terminating outlet glacier located approximately 25 km east of Kangerlussuaq (Figure 1). Following a recession for about five decades, most of the Russell Glacier margin has recently advanced 30–70 m from 1984–1999 (Knight et al., 2000). The local climate of the are (...truncated)