Antarctic subglacial lake exploration: a new frontier in microbial ecology

To date, wherever life has been sought on Earth, it has almost always been found—from high in the stratosphere (Imshenetskii et al., 1975, 1978, 1986; Wainwright et al., 2003) to deep in the

ocean trenches (Takamia et al., 1997; D'Hondt et al., 2004) and even within the Earth's crust itself (Pedersen, 2000). Microorganisms have also been found in some of the most extreme

environments. They have been found to exist in ice, boiling water, acid, salt crystals, toxic waste and even in the water cores of nuclear reactors (Rothschild and Mancinelli, 2001).

Antarctic subglacial lake ecosystems have the potential to be one of the most extreme environments on Earth, with combined stresses of high pressure, low temperature, permanent darkness,

low-nutrient availability and oxygen concentrations derived from the ice that provided the original meltwater (Siegert et al., 2003), where the predominant mode of nutrition is likely to be

chemoautotrophic. Yet, to date, the identification of significant subglacial bacterial activity in the Arctic, beneath glaciers (Skidmore et al., 2000, 2005) and in subglacial lakes (Gaidos

et al., 2004), as well as extensive work on permafrost communities and work in the deep sea, suggests that life can survive and potentially thrive in these types of environment. Microbial

life has been shown to function at gigapascal pressures (Sharma et al., 2002) and bacteria recovered from the deep ocean at around 4000 m have been shown to retain both structural integrity

and metabolic activity. They have shown activity in the Antarctic at −17 °C (Carpenter et al., 2000) and to exist in the pore spaces between ice crystals (Thomas and Dieckmann, 2002).

It has been established for some time that viable microbial life is found in glacial ice, although estimates vary widely by study, geographical location and procedure—from less than one

viable cell ml–1 in polar ice (Abyzov et al., 1982) to 6 × 107 cells ml−1 in a Greenland ice core (Sheridan et al., 2003). The identification of significant alpine subglacial bacterial

activity has already been observed (Sharp et al., 1999), and distinct bacterial communities have been characterized from beneath Arctic glaciers (Bhatia et al., 2006). Elsewhere, viable

microorganisms have been recovered from 1 million-year-old Antarctic permafrost (Kochkina et al., 2001), which makes it likely that prolonged preservation of viable microorganisms may be

prevalent in Antarctic ice-bound habitats. Thus, existing data strongly suggests that the Antarctic ice sheet may harbour a time-specific microbiological seed bank, which could provide a

source of microorganisms to inoculate subglacial environments.

The Antarctic subglacial environment described so far consists of around 145 subglacial lakes and their interconnected watercourses (Siegert, 2005; Siegert et al., 2005; Priscu et al.,

2008), although new lakes continue to be identified (Popov and Masolov, 2007; Peters et al., 2008). In Antarctic subglacial systems, 100 cells ml−1 (glacial ice) and 400 cells ml−1

(accretion or glacial transition zone ice) have been estimated from the ice above Lake Vostok (Priscu et al., 2008). Indeed, all samples in this accretion ice between 3541 and 3611 m depth

were found to contain both prokaryotic and eukaryotic microorganisms (Priscu et al., 1999; Price, 2000; Poglazova et al., 2001; Christner et al., 2001), and functional groupings have even

been described, such as the thermophilic chemoautotrophic Hydrogenophilus thermoluteolus (Lavire et al., 2006). More recently, microbes have been detected in sediments collected from beneath

the West Antarctic Ice Sheet (Lanoil et al., 2009) so the potential for microbial life in Antarctic subglacial lake systems is clear.

The estimated time of migration of microorganisms through the ice into Antarctic subglacial lakes, is of the order of 10 000–50 000 years—not long enough for the evolution of completely new

species, but certainly long enough for novel biochemical, physiological and morphological diversity to potentially exist, or for the continued existence of relic populations that may have

become extinct elsewhere. In such an extreme environment, the mere presence of life in itself would be a major scientific discovery, but there are reasons to expect that such microorganisms

would possess special or unique adaptations to this unusual and potentially hostile environment. Analysis of the metabolic activity and capability or new physiologies (using a metagenomic or

high-throughput sequencing approach) and bioenergetics through the analysis of biochemical pathways of returned samples, will help to gain a better understanding of the potential role of

such subglacial lake microorganisms in biogeochemical cycling and in their functioning and control of ecosystem processes, or indeed their biotechnological potential (Raymond et al., 2008).

In addition, the climate record locked in subglacial lake sediments has the potential to provide unique insights into past changes in ecosystem function and adaptation.

With the advent of molecular techniques, microbial ecology has entered a golden age of advancement and discovery. We have also reached the point at which technology can tackle one of the

final frontiers of exploration in the search for life on Earth. It is now financially, logistically and practically possible to study Antarctic subglacial lake systems. Significant

challenges still remain, however, particularly with respect to obtaining samples from such a remote and hostile environment, while preventing contamination (Vincent, 1999) of both the

samples themselves and the subglacial environment (either microbiologically or chemically)—particularly as Antarctic subglacial lake systems are believed to be hydraulically interconnected

(Price et al., 2002), and in the unambiguous interpretation of microbiological material obtained. However, progress is being made on each of these fronts: resources have been made available

for access at Lake Vostok and Lake Ellsworth www.nerc.ac.uk/press/releases/2009/03-ellsworth.asp (Figure 1), methods are already under development in analogous systems to effectively sample

these environments (Doran et al., 2008), particularly with respect to the potential for contamination (Alekhina et al., 2006) and an initial assessment has already been made on what is

needed to responsibly explore Antartic subglacial lake environments (National Research Council, 2007).

The location of Lake Ellsworth and Lake Vostok in West and East Antarctica, respectively.

We are now, therefore, in a position to ask some very interesting questions of these systems, such as: do the Antarctic subglacial lake environments contain life, and if so, what, where and

how? What can subglacial lake microorganisms tell us about the distribution and evolution of microbial life in on Earth? What are the biogeochemical resources of this unique gene pool? What

unique historical climate change record is locked within subglacial lake sediments, and how do Antarctic subglacial lakes interact with and influence the overlying ice sheet? To address

these questions, developments and improvements in key techniques can now be applied to subglacial lake samples. These include: microscopy; fluorescent and electron microscopy (linked to

specific gene probes), molecular biology; genomic DNA extracted from material obtained and used to construct metagenomic libraries (to screen for new physiologies), physiology and

biochemistry (to investigate biogeochemical cycling), direct culture and biomarkers or tracers (Wackett, 2007).

Advances in molecular technology have vastly improved life detection limits, such that microscopy and PCR are now capable of detecting individual cells per ml, or the DNA itself at 0.1–0.2 

μl−1. To date, 16S rDNA-based community reconstruction has shown sequences between 6–93 from Lake Vostok accretion ice (though this figure is known to include contaminants). Adopting a

culture-based approach from Antarctic ice cores, 0, 2 and 10 cfu ml−1 have been isolated from Dyer Plateau, Siple Station and Taylor Dome respectively (Christner et al., 2000), and 1–16 cfu 

ml−1 from a Dronning Maud Land ice core (Pearce, unpublished data). Radiolabelled substrates can yield uptake rates at the level of several hundred cells (Karl et al., 1999). However, not

one approach is likely to provide a complete unbiased picture of the microorganisms residing in a sample or their relative numbers, and the design of specific, clean sampling strategies is

extremely important.

Although Antarctic subglacial lakes were identified almost 40 years ago (Robin et al., 1970), we are only now at a stage where the exploration of Antarctic subglacial ecosystems is a

reality, and this will open a new frontier in microbial ecology. Initial results from Lake Vostok accretion ice, access into Arctic subglacial lakes and preliminary work with shallow

Antarctic subglacial systems, suggests we are about to enter an exciting phase in Antarctic subglacial lake research. Perhaps most significantly, if Antarctic subglacial lake ecosystems are

found to be sterile, it would be a major discovery in itself.

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