Subglacial environments provide conditions suitable for the microbial production of methane, an important greenhouse gas, which can be released from beneath the ice as a result of glacial melting. High gaseous methane emissions have recently been discovered at Russell Glacier, an outlet of the southwestern margin of the Greenland Ice Sheet, acting not only as a potential climate amplifier but also as a substrate for methane consuming microorganisms. Here, we describe the composition of the microbial assemblage exported in meltwater from the methane release hotspot at Russell Glacier and its changes over the melt season and as it travels downstream. We found that a substantial part (relative abundance 27.2% across the whole dataset) of the exported assemblage was made up of methylotrophs and that the relative abundance of methylotrophs increased as the melt season progressed, likely due to the seasonal development of the glacial drainage system. The methylotrophs were dominated by representatives of type I methanotrophs from the Gammaproteobacteria; however, their relative abundance decreased with increasing distance from the ice margin at the expense of type II methanotrophs and/or methylotrophs from the Alphaproteobacteria and Betaproteobacteria. Our results show that subglacial methane release hotspot sites can be colonized by microorganisms that can potentially reduce methane emissions.

Current address Department of Environmental and Biological Sciences University of Eastern Finland Kuopio Finland

Department of Ecology Faculty of Science Charles University Prague Czechia

Department of Ecoscience Arctic Environment Aarhus University Roskilde Denmark

Department of Geoscience and Natural Resource Management University of Copenhagen Copenhagen Denmark

Zobrazit více v PubMed

Wadham JL, Hawkings JR, Tarasov L, et al. Ice sheets matter for the global carbon cycle. Nat Commun. 2019;10:3567. doi: 10.1038/s41467-019-11394-4. PubMed DOI PMC

Vinšová P, Kohler TJ, Simpson MJ, et al. The biogeochemical legacy of arctic subglacial sediments exposed by glacier retreat. Global Biogeochem Cycles. 2022;36:e2021GB007126. doi: 10.1029/2021GB007126. DOI

Wadham JL, Bottrell S, Tranter M, Raiswell R. Stable isotope evidence for microbial sulphate reduction at the bed of a polythermal high Arctic glacier. Earth Planet Sci Lett. 2004;219:341–355. doi: 10.1016/S0012-821X(03)00683-6. DOI

Tranter M, Skidmore M, Wadham J. Hydrological controls on microbial communities in subglacial environments. Hydrol Process. 2005;19:995–998. doi: 10.1002/hyp.5854. DOI

Boyd ES, Skidmore M, Mitchell AC, et al. Methanogenesis in subglacial sediments. Environ Microbiol Rep. 2010;2:685–692. doi: 10.1111/j.1758-2229.2010.00162.x. PubMed DOI

Dieser M, Broemsen ELJE, Cameron KA, et al. Molecular and biogeochemical evidence for methane cycling beneath the western margin of the Greenland ice sheet. ISME J. 2014;8:2305–2316. doi: 10.1038/ismej.2014.59. PubMed DOI PMC

Michaud AB, Dore JE, Achberger AM, et al. Microbial oxidation as a methane sink beneath the West Antarctic Ice Sheet. Nat Geosci. 2017;10:582–586. doi: 10.1038/NGEO2992. DOI

Lamarche-Gagnon G, Wadham JL, Sherwood Lollar B, et al. Greenland melt drives continuous export of methane from the ice-sheet bed. Nature. 2019;565:73–77. doi: 10.1038/s41586-018-0800-0. PubMed DOI

Stibal M, Wadham JL, Lis GP, et al. Methanogenic potential of Arctic and Antarctic subglacial environments with contrasting organic carbon sources. Glob Chang Biol. 2012;18:3332–3345. doi: 10.1111/j.1365-2486.2012.02763.x. DOI

Wadham JL, Tranter M, Tulaczyk S, Sharp M (2008) Subglacial methanogenesis: a potential climatic amplifier? Global Biogeochem Cycles 22:2. 10.1029/2007GB002951

Wadham JL, Arndt S, Tulaczyk S, et al. Potential methane reservoirs beneath Antarctica. Nature. 2012;488:633–637. doi: 10.1038/nature11374. PubMed DOI

Christiansen JR, Jørgensen CJ. First observation of direct methane emission to the atmosphere from the subglacial domain of the Greenland Ice Sheet. Sci Rep. 2018;8:1–6. doi: 10.1038/s41598-018-35054-7. PubMed DOI PMC

Burns R, Wynn PM, Barker P, et al. Direct isotopic evidence of biogenic methane production and efflux from beneath a temperate glacier. Sci Rep. 2018;8:1–8. doi: 10.1038/s41598-018-35253-2. PubMed DOI PMC

Christiansen JR, Röckmann T, Popa ME, et al. Carbon emissions from the edge of the Greenland ice sheet reveal subglacial processes of methane and carbon dioxide turnover. J Geophys Res Biogeosciences. 2021;126:e2021JG006308. doi: 10.1029/2021JG006308. DOI

Pain AJ, Martin JB, Martin EE, et al. Heterogeneous CO2and CH4content of glacial meltwater from the Greenland Ice Sheet and implications for subglacial carbon processes. Cryosphere. 2021;15:1627–1644. doi: 10.5194/tc-15-1627-2021. DOI

Dedysh SN, Knief C (2018) Diversity and phylogeny of described aerobic methanotrophs. In: Kalyuzhnaya M, Xing XH. (eds) Methane biocatalysis: paving the way to sustainability. Springer, Cham. 10.1007/978-3-319-74866-5_2

Chistoserdova L, Kalyuzhnaya MG, Lidstrom ME. The expanding world of methylotrophic metabolism. Annu Rev Microbiol. 2009;63:477–499. doi: 10.1146/annurev.micro.091208.073600. PubMed DOI PMC

Beck DAC, Kalyuzhnaya MG, Malfatti S, et al. (2013) A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae. PeerJ 1:e23. 10.7717/peerj.23 PubMed PMC

van Grinsven S, Sinninghe Damsté JS, Harrison J, et al. Nitrate promotes the transfer of methane-derived carbon from the methanotroph Methylobacter sp. to the methylotroph Methylotenera sp. in eutrophic lake water. Limnol Oceanogr. 2021;66:878–891. doi: 10.1002/lno.11648. DOI

Cameron KA, Stibal M, Hawkings JR, et al. Meltwater export of prokaryotic cells from the Greenland ice sheet. Environ Microbiol. 2017;19:524–534. doi: 10.1111/1462-2920.13483. PubMed DOI

Vrbická K, Kohler TJ, Falteisek L, et al. Catchment characteristics and seasonality control the composition of microbial assemblages exported from three outlet glaciers of the Greenland Ice Sheet. Front Microbiol. 2022;13:4757. doi: 10.3389/fmicb.2022.1035197. PubMed DOI PMC

Lindbäck K, Pettersson R, Hubbard AL, et al. Subglacial water drainage, storage, and piracy beneath the Greenland ice sheet. Geophys Res Lett. 2015;42:7606–7614. doi: 10.1002/2015GL065393. DOI

Carrivick JL, Yde JC, Knudsen NT, Kronborg C (2018) Ice-dammed lake and ice-margin evolution during the Holocene in the Kangerlussuaq area of west Greenland. Arctic, Antarct Alp Res 50:1. 10.1080/15230430.2017.1420854

Hawkings JR, Linhoff BS, Wadham JL, et al. Large subglacial source of mercury from the southwestern margin of the Greenland Ice Sheet. Nat Geosci. 2021;14:496–502. doi: 10.1038/s41561-021-00753-w. DOI

Mankoff KD, Noël B, Fettweis X, et al. Greenland liquid water discharge from 1958 through 2019. Earth Syst Sci Data. 2020;12:2811–2841. doi: 10.5194/essd-12-2811-2020. DOI

Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–1414. doi: 10.1111/1462-2920.13023. PubMed DOI

Apprill A, Mcnally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol. 2015;75:129–137. doi: 10.3354/ame01753. DOI

Větrovský T, Baldrian P, Morais D. SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics. 2018;34:2292–2294. doi: 10.1093/bioinformatics/bty071. PubMed DOI PMC

Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Aronesty E. Comparison of sequencing utility programs. Open Bioinforma J. 2013;7:1–8. doi: 10.2174/1875036201307010001. DOI

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal. 2011;17:10. doi: 10.14806/ej.17.1.200. DOI

Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

Salter SJ, Cox MJ, Turek EM, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87. doi: 10.1186/s12915-014-0087-z. PubMed DOI PMC

Glassing A, Dowd SE, Galandiuk S, et al. Inherent bacterial DNA contamination of extraction and sequencing reagents may affect interpretation of microbiota in low bacterial biomass samples. Gut Pathog. 2016;8:24. doi: 10.1186/s13099-016-0103-7. PubMed DOI PMC

Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC

Hall TA. BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp Ser. 1999;41:95–98.

Edler D, Klein J, Antonelli A, Silvestro D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol Evol. 2021;12:373–377. doi: 10.1111/2041-210X.13512. DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696–704. doi: 10.1080/10635150390235520. PubMed DOI

Page RDM. Tree View: an application to display phylogenetic trees on personal computers. Bioinformatics. 1996;12:357–358. doi: 10.1093/bioinformatics/12.4.357. PubMed DOI

Liu C, Cui Y, Li X, Yao M (2021) Microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol 97:2. 10.1093/femsec/fiaa255 PubMed

Kahle D, Wickham H (2013) ggmap: spatial visualization with ggplot2. R Journal 5:144–161. 10.32614/rj-2013-014

De CM, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566–3574. doi: 10.1890/08-1823.1. PubMed DOI

Schloss PD, Westcott SL, Ryabin T, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–7541. doi: 10.1128/AEM.01541-09. PubMed DOI PMC

Cameron KA, Müller O, Stibal M, et al. Glacial microbiota are hydrologically connected and temporally variable. Environ Microbiol. 2020;22:3172–3187. doi: 10.1111/1462-2920.15059. PubMed DOI

Dubnick A, Kazemi S, Sharp M, et al. Hydrological controls on glacially exported microbial assemblages. J Geophys Res Biogeosciences. 2017;122:1049–1061. doi: 10.1002/2016JG003685. DOI

Kohler TJ, Vinšová P, Falteisek L, et al. Patterns in microbial assemblages exported from the meltwater of arctic and sub-arctic glaciers. Front Microbiol. 2020;11:669. doi: 10.3389/fmicb.2020.00669. PubMed DOI PMC

Yde JC, Finster KW, Raiswell R, et al. Basal ice microbiology at the margin of the Greenland ice sheet. Ann Glaciol. 2010;51:71–79. doi: 10.3189/172756411795931976. DOI

Žárský JD, Kohler TJ, Yde JC, et al. (2018) Prokaryotic assemblages in suspended and subglacial sediments within a glacierized catchment on Qeqertarsuaq (Disko Island), west Greenland. FEMS Microbiol Ecol 94:7. 10.1093/femsec/fiy100 PubMed

Christiansen JR, Romero AJB, Jørgensen NOG, et al. Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland. Biogeochemistry. 2015;122:15–33. doi: 10.1007/s10533-014-0026-7. DOI

Singleton CM, McCalley CK, Woodcroft BJ, et al. Methanotrophy across a natural permafrost thaw environment. ISME J. 2018;12:2544–2558. doi: 10.1038/s41396-018-0065-5. PubMed DOI PMC

Cadieux SB, Schütte UME, Hemmerich C, et al. Exploring methane cycling in an arctic lake in Kangerlussuaq Greenland using stable isotopes and 16S rRNA gene sequencing. Front Environ Sci. 2022;10:1817. doi: 10.3389/fenvs.2022.884133. DOI

Tavormina PL, Kellermann MY, Antony CP, et al. Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti. Mol Microbiol. 2017;103:242–252. doi: 10.1111/mmi.13553. PubMed DOI

Krause SMB, Johnson T, Karunaratne YS, et al. Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions. Proc Natl Acad Sci U S A. 2017;114:358–363. doi: 10.1073/pnas.1619871114. PubMed DOI PMC

Oswald K, Graf JS, Littmann S, et al. Crenothrix are major methane consumers in stratified lakes. ISME J. 2017;11:2124–2140. doi: 10.1038/ismej.2017.77. PubMed DOI PMC

Oshkin IY, Beck DAC, Lamb AE, et al. Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response. ISME J. 2015;9:1119–1129. doi: 10.1038/ismej.2014.203. PubMed DOI PMC

He R, Wang J, Pohlman JW, et al. Metabolic flexibility of aerobic methanotrophs under anoxic conditions in Arctic lake sediments. ISME J. 2022;16:78–90. doi: 10.1038/s41396-021-01049-y. PubMed DOI PMC

Cameron KA, Stibal M, Olsen NS, et al. Potential activity of subglacial microbiota transported to anoxic river delta sediments. Microb Ecol. 2017;74:6–9. doi: 10.1007/s00248-016-0926-2. PubMed DOI PMC