Elsevier

Advances in Space Research

Volume 48, Issue 4, 16 August 2011, Pages 697-701
Advances in Space Research

Searching for life in extreme environments relevant to Jovian’s Europa: Lessons from subglacial ice studies at Lake Vostok (East Antarctica)

https://doi.org/10.1016/j.asr.2010.11.024Get rights and content

Abstract

The objective was to estimate the genuine microbial content of ice samples from refrozen water (accretion ice) from the subglacial Lake Vostok (Antarctica) buried beneath the 4-km thick East Antarctic ice sheet. The samples were extracted by heavy deep ice drilling from 3659 m below the surface. High pressure, a low carbon and chemical content, isolation, complete darkness and the probable excess of oxygen in water for millions of years characterize this extreme environment. A decontamination protocol was first applied to samples selected for the absence of cracks to remove the outer part contaminated by handling and drilling fluid. Preliminary indications showed the accretion ice samples to be almost gas free with a low impurity content. Flow cytometry showed the very low unevenly distributed biomass while repeated microscopic observations were unsuccessful.

We used strategies of Ancient DNA research that include establishing contaminant databases and criteria to validate the amplification results. To date, positive results that passed the artifacts and contaminant databases have been obtained for a pair of bacterial phylotypes only in accretion ice samples featured by some bedrock sediments. The phylotypes included the chemolithoautotrophic thermophile Hydrogenophilus thermoluteolus and one unclassified phylotype. Combined with geochemical and geophysical considerations, our results suggest the presence of a deep biosphere, possibly thriving within some active faults of the bedrock encircling the subglacial lake, where the temperature is as high as 50 °C and in situ hydrogen is probably present.

Our approach indicates that the search for life in the subglacial Lake Vostok is constrained by a high probability of forward-contamination. Our strategy includes strict decontamination procedures, thorough tracking of contaminants at each step of the analysis and validation of the results along with geophysical and ecological considerations for the lake setting. This may serve to establish a guideline protocol for studying extraterrestrial ice samples.

Introduction

The search for evidence of life in samples from subglacial Antarctic lake environments has to overcome similar technical challenges or use similar analytical procedures to those involved in the exploration of extreme extraterrestrial environments such as Jupiter’s moon Europa. Ice samples have been extracted from a deep drilling procedure initially designed for palaeoclimatic studies at the Russian station Vostok on the East Antarctic plateau (78°S, 108°E, 3488 m a.s.l, mean surface annual temperature of ∼−55 °C) where the ice is 3750 m thick. The continuous accumulation of atmospheric snow has produced an undisturbed climate record over the first 3350 m, encompassing the last 400,000 years (Petit et al., 1998). The presence of a giant underlying lake was mapped in the 1990s (Ridley et al., 1993, Kapitsa et al., 1996). By reaching 3659 m in depth the drill penetrated from 3539 m in depth into a 200-m thick ice massif of re-frozen water attached under the glacier. By this, about 120 m of the accretion (lake) ice was extracted, allowing an unexpected window on this environment.

The subglacial Lake Vostok is huge (250 km long, 50 km wide, more than 1200 m deep), and is characterized by a ∼14 Ma period of isolation, complete darkness, high pressure (about 400 bars), in situ temperatures close to freezing, ultra-low dissolved organic carbon (DOC) content, and a probable excess of dissolved oxygen released by the ice, which melts and re-freezes at different locations, renewing the lake water (Petit et al., 2005).

The accretion ice forms a ∼210-m thick ice massif of refrozen lake water, from 3539 m in depth (Fig. 1), and the ice samples provided by deep ice coring at Vostok provide the best present-day template for searching for life in this subglacial environment. The ice massif is formed by two layers: the uppermost ice (70 m – from 3539 to 3608 m) containing millimetre-sized mica-clay inclusions (accretion ice I), and the deeper ice (∼140 m – below 3608 m) which is transparent and very clean (accretion ice II). The lake ice is devoid of air and has lost its initial content (about 8% in glacier ice). The total gas volume content is two to three orders of magnitude lower (Souchez et al., 2000, Lipenkov, pers. comm.), leading to probable micro-aerobic or anaerobic conditions. Accretion ice is enriched in 4He, originating from the bedrock (decay of Uranium series) and degassing through the deep faults (Jean Baptiste et al., 2001, Petit et al., 2005).

A key question about subglacial Antarctic lakes is their ability to support microbial life since the biomass is ultra-low and forward-contamination is a major issue. The drilling operations are heavy, and while the unbroken ice material is not porous to liquids, the outer part of the ice samples is contaminated by handling as well as by the kerosene-based drilling fluid that has to be used to counterbalance the pressure of the ice and prevent the hole from closing. Therefore, stringent decontamination procedures have to be carried out to meet chemical standards, with treatment in clean (dust-free) rooms and sterile conditions. Finally, very sensitive DNA amplification techniques are applied, and thus caution should be exercised when interpreting the results.

The objective of this study was to search for and characterize DNA signatures in Lake Vostok accretion ice. The main approach used the 16S ribosomal RNA gene sequencing constrained by Ancient DNA research criteria of authentication (Willerslev and Cooper, 2005). Chemical analyses of the ice, microscopic analysis and flow cytometry for cell enumeration were conducted in parallel.

Accretion ice contains dissolved organic carbon (DOC) as low as <20 ppbC, implying ultra-oligotrophic conditions. The chemical content is also very low in accretion ice II (less than 100 ppb for total ions) while sulphate salts and carbonates are probably present (up to 1 ppm) within the inclusions from accretion ice I (De Angelis et al., 2004).

The overall environmental conditions would restrict biota to being chemoautotrophic, and possible redox couples seem to be limited to hydrogen (probably produced by water radiolysis) and/or sulphides as reducers and electron donors, and sulphates and oxygen from sediment inclusions as electron acceptors. Carbon dioxide and possibly carbonates (which produce carbon dioxide under acidic conditions) from sediments could be used as a carbon source. Therefore, if life is present one may expect to find the DNA signature of microorganisms with properties compatible with anaerobic chemoautotrophic piezophilic psychrophiles. In the lake water body, which is probably supersaturated with oxygen, microorganisms should be ‘oxygenophilic’ (i.e. ‘oxygen-loving’) or aerobic, while being resistant to the high oxygen tension.

Section snippets

Main results

Microscopic examinations were initially conducted on thoroughly decontaminated ice samples (i.e. meeting the standards for both ice geochemistry and sterile conditions). Two samples were selected: a sample from accretion ice I (3651 m) and one from glacier ice (2054 m) as the reference. Different methods were used including specially implemented techniques (i.e. fluorescence, laser confocal and scanning electron microscopy). The results were negative and no microbial cells were identified in the

Contamination issues

Our results highlight the problem of searching for life in ice samples from refrozen water of the subglacial Lake Vostok due to the very low levels of microbial biomass resulting in the high probability of forward-contamination. To this end, a special set of indexing contaminant criteria were developed for DNA studies allowing recognition of most of the findings as contaminants (Bulat et al., 2004). The current method of reducing contamination should be based on stringent decontamination

Some lessons from life detection in Lake Vostok ice samples

The subglacial Lake Vostok may be viewed as the only extremely clean giant aquatic system on the Earth providing a unique test area for searching for tiny life indices (assumed to be DNA-based) on icy worlds such as Jupiter’s moon Europa. Keeping in mind that ‘Everything is everywhere, but the environment selects’ (de Wit and Bouvier, 2006), a global approach has to be applied. In the case of extraterrestrial samples decontamination procedures should be advanced in order to achieve and measure

Acknowledgements

Vostok ice core samples were obtained from the joint Russian, French and American Program (1989–1998) and later from the Russian national program. We acknowledge the Russian Antarctic Expedition, IPEV and OPP NSF for logistic support and the SPMI drilling team for field work. We are grateful to V.Ya. Lipenkov for providing the gas data. The work was supported in Russia by the Russian Foundation for Basic Research Project RFBR-NCNIL (S.A. Bulat) and in France by the Grant ANR-07-Blan-0223-Lac

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