Microbial oxidation as a methane sink beneath the West Antarctic Ice Sheet

Abstract

Aquatic habitats beneath ice masses contain active microbial ecosystems capable of cycling important greenhouse gases, such as methane (CH4). A large methane reservoir is thought to exist beneath the West Antarctic Ice Sheet, but its quantity, source and ultimate fate are poorly understood. For instance, O2 supplied by basal melting should result in conditions favourable for aerobic methane oxidation. Here we use measurements of methane concentrations and stable isotope compositions along with genomic analyses to assess the sources and cycling of methane in Subglacial Lake Whillans (SLW) in West Antarctica. We show that sub-ice-sheet methane is produced through the biological reduction of CO2 using H2. This methane pool is subsequently consumed by aerobic, bacterial methane oxidation at the SLW sediment–water interface. Bacterial oxidation consumes >99% of the methane and represents a significant methane sink, and source of biomass carbon and metabolic energy to the surficial SLW sediments. We conclude that aerobic methanotrophy may mitigate the release of methane to the atmosphere upon subglacial water drainage to ice sheet margins and during periods of deglaciation.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: SLW water column and sediment profiles of CH4 concentration, stable isotope composition and abundance of active methane oxidizing and methanogenic taxa.
Figure 2: CH4 stable isotope biplot for nine depths of the SLW sediment porewater (black triangles).
Figure 3: Neighbour-joining phylogenetic tree of SLW pmoA DNA sequences.
Figure 4: Chemical affinity calculations for the SLW surficial (0–2 cm) sediment.

References

  1. 1

    Kirschke, S. et al. Three decades of global methane sources and sinks. Nat. Geosci. 6, 813–823 (2013).

    Article  Google Scholar 

  2. 2

    Thauer, R. K., Kaster, A-K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579–591 (2008).

    Article  Google Scholar 

  3. 3

    Conrad, R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ. Microbiol. Rep. 1, 285–292 (2009).

    Article  Google Scholar 

  4. 4

    Wadham, J. L. et al. Potential methane reservoirs beneath Antarctica. Nature 488, 633–637 (2012).

    Article  Google Scholar 

  5. 5

    Dieser, M. et al. Molecular and biogeochemical evidence for methane cycling beneath the western margin of the Greenland Ice Sheet. ISME J. 8, 2305–2316 (2014).

    Article  Google Scholar 

  6. 6

    Wadham, J. L. et al. The potential role of the Antarctic Ice Sheet in global biogeochemical cycles. Earth Environ. Sci. Trans. R. Soc. Edinburgh 104, 55–67 (2013).

    Article  Google Scholar 

  7. 7

    Christner, B. C. et al. A microbial ecosystem beneath the West Antarctic Ice Sheet. Nature 512, 310–313 (2014).

    Article  Google Scholar 

  8. 8

    Skidmore, M. in Antarctic Subglacial Environments, Geophysical Monograph Series (eds Siegert, M. J., Kennicutt II, M. C. & Bindschandler, R. A.) 61–81 (American Geophysical Union, 2011).

    Google Scholar 

  9. 9

    Fisher, A. T., Mankoff, K. D., Tulaczyk, S. M. & Tyler, S. W. High geothermal heat flux measured below the West Antarctic Ice Sheet. Sci. Rep. 1, e1500093 (2015).

    Google Scholar 

  10. 10

    Whiticar, M. J. Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem. Geol. 161, 291–314 (1999).

    Article  Google Scholar 

  11. 11

    Coleman, D. D., Liu, C.-L. & Riley, K. M. Microbial methane in the shallow Paleozoic sediments and glacial deposits of Illinois, USA. Chem. Geol. 71, 23–40 (1988).

    Article  Google Scholar 

  12. 12

    Conrad, R. in Advances in Agronomy (ed. Sparks, S.) 1–63 (Elsevier, 2007).

    Google Scholar 

  13. 13

    Schoell, M. Multiple origins of methane in the Earth. Chem. Geol. 71, 1–10 (1988).

    Article  Google Scholar 

  14. 14

    Michaud, A. B. et al. Solute sources and geochemical processes in Subglacial Lake Whillans, West Antarctica. Geology 44, 347–350 (2016).

    Article  Google Scholar 

  15. 15

    Telling, J. et al. Rock comminution as a source of hydrogen for subglacial ecosystems. Nat. Geosci. 8, 851–855 (2015).

    Article  Google Scholar 

  16. 16

    Lin, L.-H., Slater, G. F., Sherwood Lollar, B., Lacrampe-Couloume, G. & Onstott, T. C. The yield and isotopic composition of radiolytic H2, a potential energy source for the deep subsurface biosphere. Geochim. Cosmochim. Acta 69, 893–903 (2005).

    Article  Google Scholar 

  17. 17

    Matheus Carnevali, P. B. et al. Methane sources in arctic thermokarst lake sediments on the North Slope of Alaska. Geobiology 13, 181–197 (2015).

    Article  Google Scholar 

  18. 18

    Lever, M. A. et al. Evidence for microbial carbon and sulfur cycling in deeply buried ridge flank basalt. Science 339, 1305–1308 (2013).

    Article  Google Scholar 

  19. 19

    Blazewicz, S. J., Barnard, R. L., Daly, R. A. & Firestone, M. K. Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 7, 2061–2068 (2013).

    Article  Google Scholar 

  20. 20

    Jones, S. E. & Lennon, J. T. Dormancy contributes to the maintenance of microbial diversity. Proc. Natl Acad. Sci. USA 107, 5881–5886 (2010).

    Article  Google Scholar 

  21. 21

    Achberger, A. M. et al. Microbial community structure of Subglacial Lake Whillans, West Antarctica. Front. Microbiol. 7, 1457 (2016).

    Article  Google Scholar 

  22. 22

    Grant, N. J. & Whiticar, M. J. Stable carbon isotopic evidence for methane oxidation in plumes above Hydrate Ridge, Cascadia Oregon Margin. Global Biogeochem. Cycles 16, 1124 (2002).

    Google Scholar 

  23. 23

    Coleman, D. D., Risatti, J. B. & Schoell, M. Fractionation of carbon and hydrogen isotopes by methane-oxidizing bacteria. Geochim. Cosmochim. Acta 45, 1033–1037 (1981).

    Article  Google Scholar 

  24. 24

    McDonald, I. R., Bodrossy, L., Chen, Y. & Murrell, J. C. Molecular ecology techniques for the study of aerobic methanotrophs. Appl. Environ. Microbiol. 74, 1305–1315 (2008).

    Article  Google Scholar 

  25. 25

    Knief, C. Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front. Microbiol. 6, 1346 (2015).

    Article  Google Scholar 

  26. 26

    Ho, A. et al. Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ. Microbiol. Rep. 5, 335–345 (2013).

    Article  Google Scholar 

  27. 27

    Martineau, C., Whyte, L. G. & Greer, C. W. Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl. Environ. Microbiol. 76, 5773–5784 (2010).

    Article  Google Scholar 

  28. 28

    Graef, C., Hestnes, A. G., Svenning, M. M. & Frenzel, P. The active methanotrophic community in a wetland from the High Arctic. Environ. Microbiol. Rep. 3, 466–472 (2011).

    Article  Google Scholar 

  29. 29

    He, R. et al. Shifts in identity and activity of methanotrophs in Arctic lake sediments in response to temperature changes. Appl. Environ. Microbiol. 78, 4715–4723 (2012).

    Article  Google Scholar 

  30. 30

    Shock, E. L. et al. Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA. Geochim. Cosmochim. Acta 74, 4005–4043 (2010).

    Article  Google Scholar 

  31. 31

    Amend, J. P. & Shock, E. L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 175–243 (2001).

    Article  Google Scholar 

  32. 32

    Vick-Majors, T. J. et al. Physiological ecology of microorganisms in Subglacial Lake Whillans. Front. Microbiol. 7, 1705 (2016).

    Article  Google Scholar 

  33. 33

    Trimmer, M. et al. Riverbed methanotrophy sustained by high carbon conversion efficiency. ISME J. 9, 2304–2314 (2015).

    Article  Google Scholar 

  34. 34

    Iversen, N. & Blackburn, T. H. Seasonal rates of methane oxidation in anoxic marine sediments. Appl. Environ. Microbiol. 41, 1295–1300 (1981).

    Google Scholar 

  35. 35

    Marlow, J. J. et al. Carbonate-hosted methanotrophy represents an unrecognized methane sink in the deep sea. Nat. Commun. 5, 5094 (2014).

    Article  Google Scholar 

  36. 36

    Bastviken, D., Ejlertsson, J., Sundh, I. & Tranvik, L. Methane as a source of carbon and energy for lake pelagic food webs. Ecology 84, 969–981 (2003).

    Article  Google Scholar 

  37. 37

    Lough, A. C. et al. Seismic detection of an active subglacial magmatic complex in Marie Byrd Land, Antarctica. Nat. Geosci. 6, 1031–1035 (2013).

    Article  Google Scholar 

  38. 38

    Beem, L. H., Jezek, K. C. & Van Der Veen, C. J. Basal melt rates beneath Whillans Ice Stream, West Antarctica. J. Glaciol. 56, 647–654 (2010).

    Article  Google Scholar 

  39. 39

    Yvon-Durocher, G. et al. Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507, 488–491 (2014).

    Article  Google Scholar 

  40. 40

    Priscu, J. C. et al. A microbiologically clean strategy for access to the Whillans Ice Stream subglacial environment. Antarct. Sci. 11, 1–11 (2013).

    Google Scholar 

  41. 41

    Tulaczyk, S. et al. WISSARD at Subglacial Lake Whillans, West Antarctica: scientific operations and initial observations. Ann. Glaciol. 55, 51–58 (2014).

    Article  Google Scholar 

  42. 42

    National Resource Council Exploration of Antarctic Subglacial Aquatic Environments (The National Academies Press, 2007).

  43. 43

    Riedinger, N. et al. Methane at the sediment–water transition in Black Sea sediments. Chem. Geol. 274, 29–37 (2010).

    Article  Google Scholar 

  44. 44

    Wiesenburg, D. A. & Guinasso, N. L. Jr Equilibrium solubilities of methane, carbon monoxide, and hydrogen in water and sea water. J. Chem. Eng. Data 24, 356–360 (1979).

    Article  Google Scholar 

  45. 45

    Avnimelech, Y., Ritvo, G., Meijer, L. E. & Kochba, M. Water content, organic carbon and dry bulk density in flooded sediments. Aquacult. Eng. 25, 25–33 (2001).

    Article  Google Scholar 

  46. 46

    Yarnes, C. 13C and 2H measurement of methane from ecological and geological sources by gas chromatography/combustion/pyrolysis isotope-ratio mass spectrometry. Rapid Commun. Mass Spectrom. 27, 1036–1044 (2013).

    Article  Google Scholar 

  47. 47

    Vick-Majors, T. J. Biogeochemical Processes in Antarctic Aquatic Environments: Linkages and Limitations (Montana State University, 2016).

    Google Scholar 

  48. 48

    Solorzano, L. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr. 14, 799–801 (1969).

    Article  Google Scholar 

  49. 49

    Lever, M. A. et al. A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types. Front. Microbiol. 6, 476 (2015).

    Article  Google Scholar 

  50. 50

    Paegel, B. M., Emrich, C. A., Wedemayer, G. J., Scherer, J. R. & Mathies, R. A. High throughput DNA sequencing with a microfabricated 96-lane capillary array electrophoresis bioprocessor. Proc. Natl Acad. Sci. USA 99, 574–579 (2002).

    Article  Google Scholar 

  51. 51

    Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    Article  Google Scholar 

  52. 52

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

    Article  Google Scholar 

  53. 53

    Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (Wiley-Interscience, 1996).

    Google Scholar 

  54. 54

    Parkhurst, D. L. & Appelo, C. A. J. US Geological Survey Techniques and Methods 497 (US Geological Survey, 2013).

    Google Scholar 

  55. 55

    Boetius, A. & Wenzhöfer, F. Seafloor oxygen consumption fuelled by methane from cold seeps. Nat. Geosci. 6, 725–734 (2013).

    Article  Google Scholar 

  56. 56

    LaRowe, D. E. & Amend, J. P. in Microbial Life of the Deep Biosphere (eds Kallmeyer, J. & Wagner, D.) 279–302 (Walter de Gruyter, 2014).

    Google Scholar 

  57. 57

    Osburn, M. R. et al. Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Front. Microbiol. 5, 610 (2014).

    Article  Google Scholar 

  58. 58

    Shen, L. & Chen, Z. Critical review of the impact of tortuosity on diffusion. Chem. Eng. Sci. 62, 3748–3755 (2007).

    Article  Google Scholar 

  59. 59

    Broecker, W. S. & Peng, T.-H. Gas exchange rates between air and seal. Tellus 26, 21–35 (1974).

    Article  Google Scholar 

  60. 60

    Shelley, F., Abdullahi, F., Grey, J. & Trimmer, M. Microbial methane cycling in the bed of a chalk river: oxidation has the potential to match methanogenesis enhanced by warming. Freshw. Biol. 60, 150–160 (2015).

    Article  Google Scholar 

  61. 61

    Whalen, S. C., Reeburgh, W. S. & Sandbeck, K. A. Rapid methane oxidation in a landfill cover soil. Appl. Environ. Microbiol. 56, 3405–3411 (1990).

    Google Scholar 

  62. 62

    Urmann, K., Lazzaro, A., Gandolfi, I., Schroth, M. H. & Zeyer, J. Response of methanotrophic activity and community structure to temperature changes in a diffusive CH/O counter gradient in an unsaturated porous medium. FEMS Microbiol. Ecol. 69, 202–212 (2009).

    Article  Google Scholar 

  63. 63

    Siegfried, M. R., Fricker, H. A., Carter, S. P. & Tulaczyk, S. Episodic ice velocity fluctuations triggered by a subglacial flood in West Antarctica. Geophys. Res. Lett. 43, 2640–2648 (2016).

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by National Science Foundation – Division of Polar Programs grants (0838933, 1346250, 1439774 to J.C.P.; 0838941 to B.C.C.) awarded as part of the Whillans Ice Stream Subglacial Access Research Drilling (WISSARD) project. We thank the WISSARD Science Team (see http://wissard.org for the full list of team members) for their assistance in expedition planning and with collecting and processing samples. Partial support was provided by graduate fellowships from the NSF-IGERT Program (0654336), Montana Space Grant Consortium and NSF-Center for Dark Energy Biosphere Investigations (A.B.M.); a dissertation grant from the American Association of University Women (T.J.V.-M.); a NSF-Graduate Research Fellowship (A.M.A.); and a Sêr Cymru National Research Network for Low Carbon, Energy and the Environment Grant from the Welsh Government and Higher Education Funding Council for Wales (A.C.M.). We thank R. Scherer and R. Powell for sediment cores. B.B. Jørgensen, M. A. Lever and S. Nielsen provided support and assistance with DNA extraction and pmoA/mcrA amplification. Logistics were conducted by the 139th Expeditionary Airlift Squadron of the New York Air National Guard, Kenn Borek Air, and Antarctic Support Contractor, managed by Lockheed-Martin. Hot-water drill support was provided by University of Nebraska-Lincoln and directed by F. Rack and D. Duling (chief driller). D. Blythe, J. Burnett, C. Carpenter, D. Gibson, J. Lemery, A. Melby and G. Roberts provided drill support at SLW. This is C-DEBI contribution #371.

Author information

Affiliations

Authors

Contributions

A.B.M., J.E.D., T.J.V.-M., J.C.P. and M.L.S. wrote the manuscript. A.B.M., J.E.D., M.L.S. and T.J.V.-M. conducted and analysed methane concentration and isotopic data. A.M.A., A.B.M. and B.C.C. processed, analysed and interpreted the molecular data. A.C.M. conducted thermodynamic calculations. All authors contributed to the study design, collection of samples and approved the final draft of the manuscript.

Corresponding authors

Correspondence to Alexander B. Michaud or John C. Priscu.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 545 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Michaud, A., Dore, J., Achberger, A. et al. Microbial oxidation as a methane sink beneath the West Antarctic Ice Sheet. Nature Geosci 10, 582–586 (2017). https://doi.org/10.1038/ngeo2992

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing