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A microbial ecosystem beneath the West Antarctic ice sheet

A Corrigendum to this article was published on 15 October 2014

Abstract

Liquid water has been known to occur beneath the Antarctic ice sheet for more than 40 years1, but only recently have these subglacial aqueous environments been recognized as microbial ecosystems that may influence biogeochemical transformations on a global scale2,3,4. Here we present the first geomicrobiological description of water and surficial sediments obtained from direct sampling of a subglacial Antarctic lake. Subglacial Lake Whillans (SLW) lies beneath approximately 800 m of ice on the lower portion of the Whillans Ice Stream (WIS) in West Antarctica and is part of an extensive and evolving subglacial drainage network5. The water column of SLW contained metabolically active microorganisms and was derived primarily from glacial ice melt with solute sources from lithogenic weathering and a minor seawater component. Heterotrophic and autotrophic production data together with small subunit ribosomal RNA gene sequencing and biogeochemical data indicate that SLW is a chemosynthetically driven ecosystem inhabited by a diverse assemblage of bacteria and archaea. Our results confirm that aquatic environments beneath the Antarctic ice sheet support viable microbial ecosystems, corroborating previous reports suggesting that they contain globally relevant pools of carbon and microbes2,4 that can mobilize elements from the lithosphere6 and influence Southern Ocean geochemical and biological systems7.

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Figure 1: Locator map of the WIS and SLW.
Figure 2: Phylogenetic analysis of SSU gene sequences obtained from the SLW water column, surficial sediment (0–2 cm) and drilling water.
Figure 3: Morphological diversity of microbial cells in the SLW water column.

Accession codes

Primary accessions

Sequence Read Archive

Data deposits

The SSU sequence data are deposited in the NCBI SRA database under the accession number SRP041285.

References

  1. Oswald, G. K. A. & De Robin, G. Q. Lakes beneath the Antarctic ice sheet. Nature 245, 251–254 (1973)

    Article  ADS  Google Scholar 

  2. Priscu, J. C. et al. in Polar Lakes and Rivers (eds Vincent, W. & Laybourn-Parry, J. ) Ch.7 (Oxford Univ. Press, 2008)

  3. Christner, B. C., Skidmore, M. L., Priscu, J. C., Tranter, M. & Foreman, C. M. in (eds Margesin, R., Schinner, F., Marx., J.-C. & Gerday, C. ) Psychrophiles: From Biodiversity to Biotechology pp. 51–71 (Springer, 2008)

    Book  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Fricker, H. A., Scambos, T., Bindschadler, R. & Padman, L. An active subglacial water system in West Antarctica mapped from space. Science 315, 1544–1548 (2007)

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Skidmore, M., Tranter, M., Tulaczyk, S. & Lanoil, B. Hydrochemistry of ice stream beds–evaporitic or microbial effects? Hydrol. Processes 24, 517–523 (2010)

    CAS  Google Scholar 

  7. Wadham, J. L. et al. Biogeochemical weathering under ice: size matters. Glob. Biogeochem. Cycles 24, GB3025 (2010)

    Article  ADS  CAS  Google Scholar 

  8. Wright, A. & Siegert, M. A fourth inventory of Antarctic subglacial lakes. Antarct. Sci. 24, 659–664 (2012)

    Article  ADS  Google Scholar 

  9. Priscu, J. C. et al. Geomicrobiology of subglacial ice above Lake Vostok. Science 286, 2141–2144 (1999)

    Article  CAS  PubMed  Google Scholar 

  10. Karl, D. M. et al. Microorganisms in the accreted ice of Lake Vostok. Science 286, 2144–2147 (1999)

    Article  CAS  PubMed  Google Scholar 

  11. Priscu, J. C. et al. A microbiologically clean strategy for access to the Whillans Ice Stream subglacial environment. Antarct. Sci. 25, 637–647 (2013)

    Article  ADS  Google Scholar 

  12. Bell, R. E. et al. Origin and fate of Lake Vostok water frozen to the base of the East Antarctic ice sheet. Nature 416, 307–310 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Horgan, H. J. et al. Estuaries beneath ice sheets. Geology 41, 1159–1162 (2013)

    Article  ADS  Google Scholar 

  14. Christianson, K., Jacobel, R. W., Horgan, H. J., Anandakrishnan, S. & Alley, R. B. Subglacial Lake Whillans—Ice-penetrating radar and GPS observations of a shallow active reservoir beneath a West Antarctic ice stream. Earth Planet. Sci. Lett. 331–332, 237–245 (2012)

    Article  ADS  CAS  Google Scholar 

  15. Vogel, S. W. et al. Subglacial conditions during and after stoppage of an Antarctic ice stream: is reactivation imminent? Geophys. Res. Lett. 32, L14502 (2005)

    Article  ADS  Google Scholar 

  16. Montross, S. N., Skidmore, M., Tranter, M., Kivimäki, A.-L. & Parkes, R. J. A microbial driver of chemical weathering in glaciated systems. Geology 41, 215–218 (2013)

    Article  ADS  CAS  Google Scholar 

  17. Blankenship, D. D. et al. Active volcanism beneath the West Antarctic ice-sheet and implications for ice-sheet stability. Nature 361, 526–529 (1993)

    Article  ADS  Google Scholar 

  18. Michalski, G., Bhattacharya, S. K. & Girsch, G. NOx cycle and tropospheric ozone isotope anomaly: an experimental investigation. Atmos. Chem. Phys. Discuss. 13, 9443–9483 (2013)

    ADS  Google Scholar 

  19. Hansell, D. A. & Carlson, C. A. Deep-ocean gradients in the concentration of dissolved organic carbon. Nature 395, 263–266 (1998)

    Article  ADS  CAS  Google Scholar 

  20. Christner, B. C. et al. Limnological conditions in Subglacial Lake Vostok, Antarctica. Limnol. Oceanogr. 51, 2485–2501 (2006)

    Article  ADS  Google Scholar 

  21. Azam, F. et al. Occurrence and metabolic activity of organisms under the Ross Ice Shelf, Antarctica, at Station J9. Science 203, 451–453 (1979)

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Alawi, M., Lipski, A., Sander, T., Pfeiffer, E.-M. & Spieck, E. Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic. ISME J. 1, 256–264 (2007)

    Article  CAS  PubMed  Google Scholar 

  23. Lanoil, B. et al. Bacteria beneath the West Antarctic ice sheet. Environ. Microbiol. 11, 609–615 (2009)

    Article  CAS  PubMed  Google Scholar 

  24. Takacs, C., Priscu, J. & McKnight, D. Bacterial dissolved organic carbon demand in McMurdo Dry Valley Lakes, Antarctica. Limnol. Oceanogr. 46, 1189–1194 (2001)

    Article  ADS  CAS  Google Scholar 

  25. Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl Acad. Sci. USA 107, 8818–8823 (2010)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Horrigan, S. G. Primary production under the Ross Ice Shelf, Antarctica. Limnol. Oceanogr. 26, 378–382 (1981)

    Article  ADS  CAS  Google Scholar 

  27. Priscu, J. C., Downes, M. T., Priscu, L. R., Palmisano, A. C. & Sullivan, C. W. Dynamics of ammonium oxidizer activity and nitrous oxide (N2O) within and beneath Antarctic sea ice. Mar. Ecol. Prog. Ser. 62, 37–46 (1990)

    Article  ADS  CAS  Google Scholar 

  28. Fricker, H. A. & Scambos, T. Connected subglacial lake drainage activity on lower Mercer and Whillans Ice Streams, West Antarctica, 2003–2008. J. Glaciol. 55, 303–315 (2009)

    Article  ADS  Google Scholar 

  29. Depoorter, M. A. et al. Calving fluxes and basal melt rates of Antarctic ice shelves. Nature 502, 89–92 (2013)

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Haran, T., Bohlander, J., Scambos, T. & Fahnestock, M. MODIS mosaic of Antarctica (MOA) image map. http://dx.doi.org/10.7265/N5ZK5DM5 (National Snow and Ice Data Center, 2005)

  31. Carter, S. P. & Fricker, H. A. The supply of subglacial meltwater to the grounding line of the Siple Coast, West Antarctica. Ann. Glaciol. 53, 267–290 (2012)

    Article  ADS  Google Scholar 

  32. Horgan, H. J. et al. Subglacial Lake Whillans—Seismic observations of a shallow active reservoir beneath a West Antarctic ice stream. Earth Planet. Sci. Lett. 331–332, 201–209 (2012)

    Article  ADS  CAS  Google Scholar 

  33. Siegfried, M. R., Fricker, H. A., Roberts, M., Scambos, T. A. & Tulaczyk, S. A decade of West Antarctic subglacial lake interactions from combined ICESat and CryoSat-2 altimetry. Geophys. Res. Lett. 2013GL058616,. 10.1002/2013GL058616 (2014)

  34. Priscu, J. C. LTER Limno Methods Manual – MCM_Limno_Methods_current.pdf. http://www.mcmlter.org/data/lakes/MCM_Limno_Methods_current.pdf (2013)

  35. Seeberg-Elverfeldt, J., Schlüter, M., Feseker, T. & Kölling, M. Rhizon sampling of porewaters near the sediment-water interface of aquatic systems. Limnol. Oceanogr. Methods 3, 361–371 (2005)

    Article  Google Scholar 

  36. American Public Health Association. Standard methods for the examination of water and waste water (American Public Health Society Press, 1995)

  37. Costa, A. W. et al. Analysis of atmospheric inputs of nitrate to a temperate forest ecosystem from Δ17O isotope ratio measurements. Geophys. Res. Lett. 38, L15805 (2011)

    Article  ADS  CAS  Google Scholar 

  38. Casciotti. K. L. Sigman, D. M., Galanter Hastings, M., Bohlke, J. K. & Hilkert, A. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal. Chem. 74, 4905–4912 (2002)

    Article  CAS  PubMed  Google Scholar 

  39. Kaiser, J., Hastings, M. G., Houlton, B. Z., Rockmann, T. & Sigman, D. M. Triple oxygen isotope analysis of nitrate using the denitrifier method and thermal decomposition of N2O. Anal. Chem. 79, 599–607 (2007)

    Article  CAS  PubMed  Google Scholar 

  40. Fuhrman, J. & Azam, F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar. Biol. 66, 109–120 (1982)

    Article  Google Scholar 

  41. Kirchman, D., K’nees, E. & Hodson, R. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl. Environ. Microbiol. 49, 599–607 (1985)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bell, R. T. Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine. In: Kemp, P. F., Sherr, B. F., Sherr, E. B. & Cole, J. J. (eds) Handbook of Methods in Aquatic Ecology (Lewis, 1993)

    Google Scholar 

  43. Chin-Leo, G. & Kirchman, D. Estimating bacterial production in marine waters from the simultaneous incorporation of thymidine and leucine. Appl. Environ. Microbiol. 54, 1934–1939 (1988)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kepner, R. L., Wharton, R., Jr & Suttle, C. A. Viruses in Antarctic Lakes. Limnol. Oceanogr. 43, 1754–1761 (1998)

    Article  ADS  PubMed  Google Scholar 

  45. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Holland, H. D. The Chemistry of the Atmosphere and Oceans (Wiley, 1978)

    Google Scholar 

  50. Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W. & Huse, S. M. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4, e6372 (2009)

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The Whillans Ice Stream Subglacial Access Research Drilling (WISSARD) project was funded by National Science Foundation grants (0838933, 0838896, 0838941, 0839142, 0839059, 0838885, 0838855, 0838763, 0839107, 0838947, 0838854, 0838764 and 1142123) from the Division of Polar Programs. Partial support was also provided by funds from NSF award 1023233 (B.C.C.), NSF award 1115245 (J.C.P.), the NSF’s Graduate Research Fellowship Program (1247192; A.M.A.), the Italian National Antarctic Program (C.B.), and fellowships from the NSF’s IGERT Program (0654336) and the Montana Space Grant Consortium (A.B.M.). Logistics were provided by the 139th Expeditionary Airlift Squadron of the New York Air National Guard, Kenn Borek Air, and by many dedicated individuals working as part of the Antarctic Support Contractor, managed by Lockheed-Martin. The drilling was directed by F. Rack; D. Blythe, J. Burnett, C. Carpenter, D. Duling (chief driller), D. Gibson, J. Lemery, A. Melby and G. Roberts provided drill support at SLW. L. Geng, B. Vandenheuvel, A. Schauer and E. Steig provided assistance with the stable isotopic analyses. We thank J. Dore for assistance with the nutrient analysis.

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The manuscript was written by B.C.C. and J.C.P.; A.M.A. generated and analysed the molecular data; C.B., A.C.M. and M.L.S. conducted and interpreted the chemical measurements; S.P.C. and K.C. provided geophysical data; J.A.M. obtained and examined the CTD data; A.B.M. and T.J.V. contributed and analysed physiological and biogeochemical data; M.L.S. conducted and interpreted the isotopic analyses; and T.J.V. provided the micrographs. All authors contributed to the study design and acquisition of samples and/or data.

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Correspondence to Brent C. Christner or John C. Priscu.

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Extended data figures and tables

Extended Data Table 1 Crustal and seawater components to SLW waters
Extended Data Table 2 Summary of parameters for the SLW SSU gene sequence data

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Christner, B., Priscu, J., Achberger, A. et al. A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512, 310–313 (2014). https://doi.org/10.1038/nature13667

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