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Antarctic Subglacial Lake Exploration: a New Frontier in Microbial Ecology

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Antarctic Subglacial Lake Exploration: a New Frontier in Microbial Ecology The ISME Journal (2009) 3, 877–880 & 2009 International Society for Microbial Ecology All rights reserved 1751-7362/09 $32.00 www.nature.com/ismej COMMENTARY Antarctic subglacial lake exploration: a new frontier in microbial ecology DA Pearce The ISME Journal (2009) 3, 877–880; doi:10.1038/ Arctic glaciers (Bhatia et al., 2006). Elsewhere, ismej.2009.53; published online 11 June 2009 viable microorganisms have been recovered from 1 million-year-old Antarctic permafrost (Kochkina et al., 2001), which makes it likely that prolonged To date, wherever life has been sought on Earth, preservation of viable microorganisms may be it has almost always been found—from high in prevalent in Antarctic ice-bound habitats. Thus, the stratosphere (Imshenetskii et al., 1975, 1978, existing data strongly suggests that the Antarctic ice 1986; Wainwright et al., 2003) to deep in the ocean sheet may harbour a time-specific microbiological trenches (Takamia et al., 1997; D’Hondt et al., 2004) seed bank, which could provide a source of micro- and even within the Earth’s crust itself (Pedersen, organisms to inoculate subglacial environments. 2000). Microorganisms have also been found in The Antarctic subglacial environment described some of the most extreme environments. They have so far consists of around 145 subglacial lakes and been found to exist in ice, boiling water, acid, salt their interconnected watercourses (Siegert, 2005; crystals, toxic waste and even in the water cores of Siegert et al., 2005; Priscu et al., 2008), although nuclear reactors (Rothschild and Mancinelli, 2001). new lakes continue to be identified (Popov and Antarctic subglacial lake ecosystems have the Masolov, 2007; Peters et al., 2008). In Antarctic potential to be one of the most extreme environ- subglacial systems, 100 cells mlÀ1 (glacial ice) and ments on Earth, with combined stresses of high 400 cells mlÀ1 (accretion or glacial transition zone pressure, low temperature, permanent darkness, ice) have been estimated from the ice above Lake low-nutrient availability and oxygen concentrations Vostok (Priscu et al., 2008). Indeed, all samples derived from the ice that provided the original in this accretion ice between 3541 and 3611 m meltwater (Siegert et al., 2003), where the predomi- depth were found to contain both prokaryotic and nant mode of nutrition is likely to be chemoauto- eukaryotic microorganisms (Priscu et al., 1999; trophic. Yet, to date, the identification of significant Price, 2000; Poglazova et al., 2001; Christner et al., subglacial bacterial activity in the Arctic, beneath 2001), and functional groupings have even been glaciers (Skidmore et al., 2000, 2005) and in described, such as the thermophilic chemoauto- subglacial lakes (Gaidos et al., 2004), as well as trophic Hydrogenophilus thermoluteolus (Lavire extensive work on permafrost communities and et al., 2006). More recently, microbes have been work in the deep sea, suggests that life can survive detected in sediments collected from beneath and potentially thrive in these types of environment. the West Antarctic Ice Sheet (Lanoil et al., 2009) so Microbial life has been shown to function at the potential for microbial life in Antarctic sub- gigapascal pressures (Sharma et al., 2002) and glacial lake systems is clear. bacteria recovered from the deep ocean at around The estimated time of migration of microorgan- 4000 m have been shown to retain both structural isms through the ice into Antarctic subglacial lakes, integrity and metabolic activity. They have shown is of the order of 10 000–50 000 years—not long activity in the Antarctic at À17 1C (Carpenter et al., enough for the evolution of completely new species, 2000) and to exist in the pore spaces between ice but certainly long enough for novel biochemical, crystals (Thomas and Dieckmann, 2002). physiological and morphological diversity to poten- It has been established for some time that viable tially exist, or for the continued existence of relic microbial life is found in glacial ice, although populations that may have become extinct else- estimates vary widely by study, geographical loca- where. In such an extreme environment, the mere tion and procedure—from less than one viable presence of life in itself would be a major scientific cell ml–1 in polar ice (Abyzov et al., 1982) to discovery, but there are reasons to expect that such 6 Â 107 cells mlÀ1 in a Greenland ice core (Sheridan microorganisms would possess special or unique et al., 2003). The identification of significant alpine adaptations to this unusual and potentially hostile subglacial bacterial activity has already been ob- environment. Analysis of the metabolic activity and served (Sharp et al., 1999), and distinct bacterial capability or new physiologies (using a metage- communities have been characterized from beneath nomic or high-throughput sequencing approach) Commentary 878 and bioenergetics through the analysis of biochem- interpretation of microbiological material obtained. ical pathways of returned samples, will help to gain However, progress is being made on each of these a better understanding of the potential role of such fronts: resources have been made available for subglacial lake microorganisms in biogeochemical access at Lake Vostok and Lake Ellsworth www.nerc. cycling and in their functioning and control of ac.uk/press/releases/2009/03-ellsworth.asp (Figure 1), ecosystem processes, or indeed their biotechnological methods are already under development in analo- potential (Raymond et al., 2008). In addition, the gous systems to effectively sample these environ- climate record locked in subglacial lake sediments ments (Doran et al., 2008), particularly with respect has the potential to provide unique insights into to the potential for contamination (Alekhina et al., past changes in ecosystem function and adaptation. 2006) and an initial assessment has already been With the advent of molecular techniques, micro- made on what is needed to responsibly explore bial ecology has entered a golden age of advance- Antartic subglacial lake environments (National ment and discovery. We have also reached the point Research Council, 2007). at which technology can tackle one of the final We are now, therefore, in a position to ask some frontiers of exploration in the search for life on very interesting questions of these systems, such as: Earth. It is now financially, logistically and practi- do the Antarctic subglacial lake environments cally possible to study Antarctic subglacial lake contain life, and if so, what, where and how? What systems. Significant challenges still remain, how- can subglacial lake microorganisms tell us about the ever, particularly with respect to obtaining samples distribution and evolution of microbial life in on from such a remote and hostile environment, while Earth? What are the biogeochemical resources of this preventing contamination (Vincent, 1999) of both unique gene pool? What unique historical climate the samples themselves and the subglacial environ- change record is locked within subglacial lake ment (either microbiologically or chemically)— sediments, and how do Antarctic subglacial lakes particularly as Antarctic subglacial lake systems interact with and influence the overlying ice sheet? are believed to be hydraulically interconnected To address these questions, developments and (Price et al., 2002), and in the unambiguous improvements in key techniques can now be Figure 1 The location of Lake Ellsworth and Lake Vostok in West and East Antarctica, respectively. The ISME Journal Commentary 879 applied to subglacial lake samples. These include: Christner BC, Mosley-Thompson E, Thompson LG, microscopy; fluorescent and electron microscopy Reeve JN. (2001). Isolation of bacteria and 16S rDNAs (linked to specific gene probes), molecular biology; from Lake Vostok accretion ice. Environ Microbiol 3: genomic DNA extracted from material obtained and 570–577. used to construct metagenomic libraries (to screen Christner BC, Mosley-Thompson E, Thompson LG, Zagor- odnov V, Sandman K, Reeve JN. (2000). Recovery and for new physiologies), physiology and biochemistry identification of viable bacteria immured in glaical (to investigate biogeochemical cycling), direct cul- ice. Icarus 144: 479–485. ture and biomarkers or tracers (Wackett, 2007). D’Hondt S, Jørgensen B-B, Miller DJ, Batzke A, Blake R, Advances in molecular technology have vastly Cragg BA et al. (2004). Distributions of microbial improved life detection limits, such that microscopy activities in deep sub-seafloor sediments. Science 306: and PCR are now capable of detecting individual 2216. cells per ml, or the DNA itself at 0.1–0.2 mlÀ1.To Doran PT, Fritsen CH, Murray AE, Kenig F, Mckay CP, date, 16S rDNA-based community reconstruction Kyne JD. (2008). Entry approach into pristine ice- has shown sequences between 6–93 from Lake sealed lakes—Lake Vida, East Antarctica, a model Vostok accretion ice (though this figure is known ecosystem. Limn Oceanogr Meth 6: 542–547. Gaidos E, Lanoil B, Thorsteinsson T, Graham A, Skidmore to include contaminants). Adopting a culture-based M, Han S-K et al. (2004). A viable microbial commu- approach from Antarctic ice cores, 0, 2 and nity in a subglacial volcanic crater lake, Iceland. À1 10 cfu ml have been isolated from Dyer Plateau, Astrobiol 4: 327–344. Siple Station and Taylor Dome respectively (Christ- Imshenetskii AA, Lysenko SV, Kazakov GA. (1975). ner et al., 2000), and 1–16 cfu mlÀ1 from a Dronning Microorganisms of stratosphere. Doklady Akademii
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