Microbial Life beneath a High Arctic Glacier<sup><a href="#FN151" rid="FN151" class=" fn">†</a></sup>

Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E3,^{and Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9}²

^{Corresponding author. Present address: Bristol Glaciology Centre, School of Geographical Sciences, University of Bristol, University Road, Bristol, BS8 1SS, United Kingdom. Phone: (44) (117) 928 8186. Fax: (44) (117) 928 7878. E-mail:}ku.ca.lotsirb@eromdikS.kraM.

Received 2000 Jan 27; Accepted 2000 May 26.

Abstract

The debris-rich basal ice layers of a high Arctic glacier were shown to contain metabolically diverse microbes that could be cultured oligotrophically at low temperatures (0.3 to 4°C). These organisms included aerobic chemoheterotrophs and anaerobic nitrate reducers, sulfate reducers, and methanogens. Colonies purified from subglacial samples at 4°C appeared to be predominantly psychrophilic. Aerobic chemoheterotrophs were metabolically active in unfrozen basal sediments when they were cultured at 0.3°C in the dark (to simulate nearly in situ conditions), producing ^CO₂ from radiolabeled sodium acetate with minimal organic amendment (≥38 μM C). In contrast, no activity was observed when samples were cultured at subfreezing temperatures (≤−1.8°C) for 66 days. Electron microscopy of thawed basal ice samples revealed various cell morphologies, including dividing cells. This suggests that the subglacial environment beneath a polythermal glacier provides a viable habitat for life and that microbes may be widespread where the basal ice is temperate and water is present at the base of the glacier and where organic carbon from glacially overridden soils is present. Our observations raise the possibility that in situ microbial production of CO₂ and CH₄ beneath ice masses (e.g., the Northern Hemisphere ice sheets) is an important factor in carbon cycling during glacial periods. Moreover, this terrestrial environment may provide a model for viable habitats for life on Mars, since similar conditions may exist or may have existed in the basal sediments beneath the Martian north polar ice cap.

Abstract

Microbial activity has been found in ice-sediment communities in the surface layers of perennial and permanent lake ice at a depth of 2 m (30, 31). The lake ice microbial consortia are dependent on photosynthesis to provide energy for growth. In subglacial environments bacterial populations have been found beneath alpine glaciers (35) and in subglacially accreted ice above Lake Vostok, Antarctica (20, 29). However, the biogeochemical function of these populations has not been determined, and it remains to be demonstrated that they are active at in situ subglacial temperatures and under in situ conditions. Clearly, active subglacial microbial populations would have to be chemotrophic (nonphotosynthetic). Demonstrating the viability and geochemical function of subglacial microbial populations has a number of important consequences.

First, the presence of viable chemotrophic microbial activity at low temperatures (0 to 4°C) has important implications for global carbon cycling calculations. Traditionally, it has been thought that continental glaciation results in cessation of geochemical processes beneath the ice (13), and the impact of subglacial microbially mediated weathering has received little consideration. However, during the last glacial maximum, ice sheets covered approximately 20% of the continental northern hemisphere (16, 23, 24), including the area that is currently covered by the boreal forest, the world's largest store of soil carbon, whose size is estimated to be 330 Pg (40). A similar distribution of vegetation has been proposed for the last interglacial period (Eemian), as recorded in glacially overridden soils and peat (10, 32) and paleosols in unglaciated terrain beyond the ice margin (26). These overridden soils and peat deposits provide a large source of organic carbon beneath the midlatitude ice sheets. A number of the current carbon cycle models assume that the carbon accumulated during the Eemian in areas covered by the ice sheets was returned to the atmosphere by the last glacial maximum (1, 12, 40), but there has been no explanation as to how this was achieved. Ice is an efficient erosive agent (2, 15), and, therefore, it is likely that some of the carbon may be moved by physical transport to the ice sheet margins, either in ice, in deforming sediments, or in meltwater. However, active biogeochemical oxidation or reduction of the remaining carbon beneath warm-based sectors of midlatitude ice sheets may have a significant impact on carbon budget calculations for continental regions during the glacial phase of a glacial-interglacial cycle. Moreover, low-temperature respiration and/or fermentation of organic carbon in the subsurface environments of periglacial (33, 41) soils in unglaciated midlatitude regions and ice marginal zones is potentially an important process that previously has been given little consideration on glacial-interglacial time scales.

Second, extreme polar terrestrial environments are being investigated as analogues of viable extraterrestrial habitats (3, 14). Currently, water on Mars has been observed only as ice in the two polar caps (8). Given that all known bacteria on Earth require liquid water to be metabolically active, some of the most likely potential habitats for microbial life on Mars are the polar environments (36). Moreover, subglacial environments could provide shelter from the harsh conditions at the planet's surface, including large diurnal and seasonal temperature fluctuations and strong UV radiation. Some models suggest that during times of high obliquity on Mars, surficial melting may have occurred in the north polar ice cap (28). Under these conditions, the ice cap may have exhibited polythermal conditions and may have been more dynamic (19), and thus basal melting may have occurred, producing sediment-rich basal ice. Hence, debris-rich ice exposed at the margins of the north polar ice cap or as part of polar layered deposits may provide a record of dormant or possibly extant microbial life that is relatively accessible.

In this study we performed a number of laboratory experiments in which we assessed the diversity and viability of microbes from a high Arctic glaciated environment and examined the effects of microbial activity on biogeochemical processes. In the experiments we also compared microbial population diversity in surficial glacier environments (supraglacial waters and glacier ice, which are characterized by low solute concentrations [<10 μS cm^{] and low sediment concentrations [<0.01 g liter}^{]) with microbial population diversity in subglacial environments (subglacial meltwaters and basal ice, which are characterized by high solute concentrations [>100 μS cm}^{] and high sediment concentrations [>0.1 g liter}^]).

ACKNOWLEDGMENTS

This research was supported by Canadian Circumpolar Institute and Geological Society of America grants to M. L. Skidmore and by NSERC operating grants to J. M. Foght and M. J. Sharp. Logistical field support was provided by the Polar Continental Shelf Project (PCSP), Canada.

Fieldwork was carried out with permission from the Nunavut Research Institute and the hamlets of Grise Fjord and Resolute Bay. R. Young, J. Barker, L. Copland, W. Davis, and D. Glowacki assisted in the collection of field samples, S. Ebert provided technical help with the culture work, and R. Bhatnagar assisted with the TEM imaging. DOC and TOC analyses of the ice samples were kindly performed by K. Leckrone, Biogeochemical Laboratories, Indiana University. We are grateful to K. Muehlenbachs for helpful discussions and to two anonymous referees for their comments.

ACKNOWLEDGMENTS

Footnotes

^{This is Polar Continental Shelf Project contribution 00199.}

Footnotes

REFERENCES

References

1. Adams J M, Faure H, Faure-Denard L, McGlade J M, Woodward F IIncreases in the terrestrial carbon storage from the Last Glacial Maximum to the present. Nature. 1990;348:711–714.[PubMed][Google Scholar]
2. Alley R B, Cuffey K M, Evenson E B, Strasser J C, Lawson D E, Larson G JHow glaciers entrain and transport basal sediment: physical constraints. Quat Sci Rev. 1997;16:1017–1038.[PubMed][Google Scholar]
3. Andersen D T, Pollard W H, McKay C T, Omelon CPerennial springs in the Canadian High Arctic, analogs of past Martian liquid water habitats. Eos Trans. 1998;79(45):59.[PubMed][Google Scholar]
4. Arendt A M. S. thesis. Alberta, Edmonton, Canada: University of Alberta; 1997. [PubMed][Google Scholar]
5. Atlas R M Handbook of microbiological media for environmental microbiology. Boca Raton, Fla: CRC Press; 1995. [PubMed][Google Scholar]
6. Bengtsson L, Enell M. Chemical analysis. In: Berglund B E, editor. Handbook of Holocene palaeoecology and palaeohydrology. Chichester, United Kingdom: Wiley-Interscience; 1986. pp. 423–451. [PubMed]
7. Butlin K R, Adams M E, Thomas MThe isolation and cultivation of sulfate-reducing bacteria. J Gen Microbiol. 1949;3:46–59.[PubMed][Google Scholar]
8. Cantor B A, James P B Proceedings of the 1st International Conference on Mars Polar Science and Exploration. Lunar and Planetary Institute contribution no. 953. Houston, Tex: Lunar and Planetary Institute; 1998. Review of the 1990–1997 Hubble space telescope observations of the Martian polar caps; pp. 5–6. [PubMed][Google Scholar]
9. Clifford S MPolar basal melting on Mars. J Geophy Res. 1987;92:9135–9152.[PubMed][Google Scholar]
10. Dredge L A, Morgan A V, Nielsen ESangamon and pre-Sangamon interglaciations in the Hudson Bay lowlands of Manitoba. Geogr Phys Quat. 1990;44:319–336.[PubMed][Google Scholar]
11. Fedorak P M, Foght J M, Westlake D W SA method for monitoring mineralization of ^{C-labeled compounds in aqueous samples.}Water Res. 1982;16:1285–1290.[PubMed][Google Scholar]
12. Francois L M, Godderis Y, Warnant P, Ramstein G, de Noblet N, Lorenz SCarbon stocks and isotopic budgets of the terrestrial biosphere at mid-Holocene and last glacial maximum times. Chem Geol. 1999;159:163–189.[PubMed][Google Scholar]
13. Gibbs M T, Kump L RGlobal chemical erosion during the last glacial maximum and the present: sensitivity to changes in lithology and hydrology. Paleoceanography. 1994;9:529–543.[PubMed][Google Scholar]
14. Gilichinsky D A, Soina V S, Petrova V ACryoprotective properties of water in the earth cryolithosphere and its role in exobiology. Origins Life Evol Biosphere. 1993;23:65–75.[PubMed][Google Scholar]
15. Hallet B, Hunter L, Bogen JRates of erosion and sediment evacuation by glaciers: a review of field data and their implications. Global Planet Change. 1996;12:213–235.[PubMed][Google Scholar]
16. Holmlund P, Fastook JA time dependent glaciological model of the Weichselian Ice Sheet. Quat Int. 1995;27:53–58.[PubMed][Google Scholar]
17. Hubbard B, Sharp M JBasal ice formation and deformation: a review. Prog Phys Geogr. 1989;13:529–558.[PubMed][Google Scholar]
18. Iverson N R, Semmens D JIntrusion of ice into porous media by regelation: a mechanism of sediment entrainment by glaciers. J Geophy Res. 1995;100:10219–10230.[PubMed][Google Scholar]
19. Kargel J S Proceedings of the 1st International Conference on Mars Polar Science and Exploration. Lunar and Planetary Institute contribution no. 953. Houston, Tex: Lunar and Planetary Institute; 1998. Possible composition of Martian polar caps and controls on ice-cap behaviour; pp. 22–23. [PubMed][Google Scholar]
20. Karl D M, Bird D F, Bjorkman K, Houlihan T, Shackelford R, Tupas LMicroorganisms in the accreted ice of Lake Vostok, Antarctica. Science. 1999;286:2144–2147.[PubMed][Google Scholar]
21. Lawson D E, Strasser J C, Evenson E B, Alley R B, Larson G J, Arcone S A. Glaciohydraulic supercooling: a freeze-on mechanism to create stratified, debris-rich ice. I. Field evidence. J Glaciol. 1999;44:547–562.[PubMed]
22. Leckrone K J Ph.D. thesis. Bloomington: University of Indiana; 1997. [PubMed][Google Scholar]
23. Ludwig W, Amiotte-Suchet P, Probst J-LEnhanced chemical weathering of rocks during the last glacial maximum: a sink for atmospheric CO₂? Chem Geol. 1999;159:147–161.[PubMed][Google Scholar]
24. Marshall S J, Clarke G K CModeling North American fresh water runoff through the last glacial cycle. Quat Res. 1999;52:300–315.[PubMed][Google Scholar]
25. Mikesell M D, Kukor J J, Olsen R HMetabolic diversity of aromatic hydrocarbon-degrading bacteria from a petroleum-contaminated aquifer. Biodegradation. 1993;4:249–259.[PubMed][Google Scholar]
26. Morozova T D, Velichko A A, Dlussky K GOrganic carbon content in the late Pleistocene and Holocene fossil soils (reconstruction for Eastern Europe) Global Planet Change. 1998;16–17:131–151.[PubMed][Google Scholar]
27. Paterson W S B The physics of glaciers. 1st ed. Oxford, United Kingdom: Pergamon; 1969. [PubMed][Google Scholar]
28. Pathare A V, Paige D A Proceedings of the 1st International Conference on Mars Polar Science and Exploration. Lunar and Planetary Institute contribution no. 953. Houston, Tex: Lunar and Planetary Institute; 1998. Recent liquid water in the polar regions of Mars; pp. 31–32. [PubMed][Google Scholar]
29. Priscu J C, Adams E E, Berry Lyons W, Voytek M A, Mogk D W, Brown R L, McKay C P, Takacs C D, Welch K A, Wolf C F, Kirshtein J D, Avci RGeomicrobiology of subglacial ice above Lake Vostok, Antarctica. Science. 1999;286:2141–2144.[PubMed][Google Scholar]
30. Priscu J C, Fritsen C H, Adams E E, Giovannoni S J, Paerl H W, McKay C P, Doran P T, Gordon D A, Lanoil B D, Pinckney J LPerennial Antarctic lake ice: an oasis for life in a polar desert. Science. 1998;280:2095–2098.[PubMed][Google Scholar]
31. Psenner R, Sattler BLife at the freezing point. Science. 1998;280:2073–2074.[PubMed][Google Scholar]
32. Punkari M, Forsstrom LOrganic remains in Finnish subglacial sediments. Quat Res. 1995;43:415–425.[PubMed][Google Scholar]
33. Rivkina E, Gilichinsky D, Wagener S, Tiedje J, McGrath JBiogeochemical activity of anaerobic microorganisms from buried permafrost sediments. Geomicrobiology. 1998;15:187–193.[PubMed][Google Scholar]
34. Sagemann J, Jorgensen B B, Greeff OTemperature dependence and rates of sulfate reduction in cold sediments of Svalbard, Arctic Ocean. Geomicrobiol J. 1998;15:85–100.[PubMed][Google Scholar]
35. Sharp M, Parkes J, Cragg B, Fairchild I J, Lamb H, Tranter MWidespread bacterial populations at glacier beds and their relationship to rock weathering and carbon cycling. Geology. 1999;27:107–110.[PubMed][Google Scholar]
36. Skidmore M, Foght J M, Sharp M J Proceedings of the 1st International Conference on Mars Polar Science and Exploration. Lunar and Planetary Institute contribution no. 953. Houston, Tex: Lunar and Planetary Institute; 1998. Microbial experiments on basal ice from John Evans Glacier, eastern Ellesmere Island, N.W.T., Canada; pp. 34–35. [PubMed][Google Scholar]
37. Skidmore M L, Sharp M JDrainage behaviour of a high Arctic polythermal glacier. Ann Glaciol. 1999;28:209–215.[PubMed][Google Scholar]
38. Souchez R, Bouzette A, Clausen H B, Johnsen S J, Jouzel JA stacked mixing sequence at the base of the Dye 3 core, Greenland. Geophys Res Lett. 1998;25:1943–1946.[PubMed][Google Scholar]
39. Souchez R, Lemmens M, Chappellaz JFlow-induced mixing in the GRIP basal ice deduced from the CO₂ and CH₄ records. Geophys Res Lett. 1995;22:41–44.[PubMed][Google Scholar]
40. Van Campo E, Guiot J, Peng CA data-based reappraisal of the terrestrial carbon budget at the last glacial maximum. Global Planet Change. 1993;8:189–201.[PubMed][Google Scholar]
41. Zimov S A, Zimova G M, Daviodov S P, Daviodova A I, Voropaev Y V, Voropaeva Z V, Prosiannikov S F, Prosiannikova O V, Semiletova I V, Semiletov I PWinter biotic activity and production of CO₂ in Siberian soils: a factor in the greenhouse effect. J Geophys Res. 1993;98:5017–5023.[PubMed][Google Scholar]
42. Zinder S H. Physiological ecology of methanogens. In: Ferry J G, editor. Methanogenesis. New York, N.Y: Chapman and Hall; 1993. pp. 128–206. [PubMed]