Subglacial Environments: Biological Features
BIOLOGY—CONCLUSIONS Summary
The subglacial aquatic environments of the Antarctic lie beneath kilometers of ice.
Microbes of a number of types are found in low numbers throughout all depths of the ice sheet, carried to the Antarctic by atmospheric winds and deposited at the surface.
Some of these survive their extremely slow downward travel through the ice and are still capable of respiration and growth when sampled in cores from thousands of meters below the surface. It is, therefore, highly likely that the subglacial aquatic environments contain microbes capable of growth and are constantly being inoculated with microbes from the ice sheet. The important question then centers on the probability that these environments support growing and evolving microbial populations. After consider-ing the requirements for microbial growth and the chemical and physical conditions predicted for subglacial environments, the committee concluded that the hypothesis of microbial life and growth cannot be rejected. Therefore, future exploration of these environments must assume an aquatic ecosystem containing growing microbial popu-lations. This assumption affects issues of preservation of habitats and minimization of contamination during exploration. The uncertainty can be resolved only by direct sampling of the lakes and flowing waters beneath the ice sheet.
Requirements for Life
The proliferation of microorganisms requires, at a minimum an inoculum of cells;
water; electron donors and acceptors (e.g., reduced iron, sulfides, organic matter, oxygen) for biological energy supply; a source of nutrients (e.g., C, N, P, S, Fe, and other elemental constituents of biomolecules); sufficient time for reproduction; and the physical, chemical, or biological conditions that prevent cell destruction and promote growth. Subglacial aquatic environments have not been studied directly; therefore no unequivocal evidence exists to confirm the presence or absence of life in these ecosystems.
Subglacial Aquatic Environments and Potential Microbial Communities Two types of evidence have been used to predict what will be found in waters beneath the ice sheet. First, microbes exist in all extreme environments on Earth where there is water, from a depth of 10,000 m in the ocean to surface saline lakes and from subzero temperatures in the brine channels of ocean ice to hot springs. Subsurface microbial communities of land and ocean are driven by abiotically produced materials from the Earth’s interior such as sulfides, hydrogen, and carbon dioxide. Based on this, it appears likely that actively growing microbes will be present in subglacial waters.
Second, although Lake Vostok has not been studied directly, there are samples of the chemistry and microbiology of the ice that has been derived from the lake (accreted ice); these indicate that there are no environmental conditions that would rule out microbial life within the lake.
SUBGLACIAL ENVIRONMENTS: BIOLOGICAL FEATURES
Another complication for predicting the present conditions in the subglacial waters is that rock particles from glacial scour and sediments from preglacial lakes might be present. These materials could be sources for biota as well as for electron donors and acceptors for chemotrophic and heterotrophic organisms.
No matter what their origin, the substrates required for microbial growth appear to be present in the water column of subglacial aquatic systems at low concentrations, although a richer microbial habitat may be provided in the underlying sediments. The supply rate of these substrates is one of the key unknowns; however, the concentrations of growth substrates are considered to be low, suggesting that these environments are oligotrophic. As a consequence, microbes adapted to these environments by necessity will most likely have highly proficient metabolic processes capable of taking advantage of extremely oligotrophic conditions including efficient recycling strategies. Depending on the level of carbon and nutrients available to the microbial community, metabolic activity and growth could be very low in some aquatic environments and some fraction of the community may represent a viable but metabolically inactive state. It is likely that microbial communities, if present and active, will only be able to grow extremely slowly.
The growth of accretion ice in Lake Vostok may have created an environment where oxygen concentrations are 50 times higher than in normal lake waters. This situation is likely to occur because enclathrated hydrates of atmospheric air contained in glacial ice are released into the lake when this ice melts. Accretion ice excludes gases as it grows; the result is supersaturation of the upper levels of the lake water with gases.
Unless the gases are removed by mixing into the deep waters or by transport out of the lake, high concentrations of oxygen may result in the production of superoxide radicals and other reactive oxygen species that could be detrimental to life. Alternatively, if the subglacial lakes are stratified there may be low oxygenic levels and anoxic bottom waters and sediments where microbes could exist.
Microbes in Glacial Ice and Subglacial Waters
The microbes in glacial and accretion ice have been examined by several methods.
Microscopic and culture analysis of the Vostok ice core revealed bacteria, yeasts, fungi, and microalgae in glacial ice greater than 240,000 years old. In the oldest ice, only bacterial spores were found. Microbiological and molecular-based studies of the accretion ice found low but detectable amounts of bacterial cells and DNA. Molecular identification of microbes show that they are closely related to microbiota from the surface of the Earth: Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes.
Microscopic examination revealed bacteria, pollen, diatoms, and coccolithophorids.
Of these, only the bacteria would be able to grow in the lake water.
Bacteria and yeasts from the accretion ice, thus presumably from Lake Vostok, respired glucose and grew on liquid and agar media. The total numbers of micro-organisms detected in the accretion ice ranged from 100 to 900 cells mL–1.
Actual growth rates are unknown for bacteria in subglacial ecosystems, but are expected to be slow and possibly negligible in some situations. Analogous systems include the deep subseafloor biosphere, where one report estimated that the bacterial turnover time is up to 22 years (Schippers et al. 2005). These slow rates of metabolism and growth also have implications for the extent of genetic adaptation to the subglacial
0 EXPLORATION OF ANTARCTIC SUBGLACIAL AQUATIC ENVIRONMENTS
environment given that rates of evolution tend to be slow under conditions of low temperature (Gillooly et al. 2005) and low productivity (Horner-Devine et al. 2003).
The Possibility of Microbial Evolution
If the source population of microbial communities in subglacial aquatic environ-ments is derived from the overlying glacial ice, these populations have been isolated for at least 1 million years, which is the age of the oldest Antarctic ice. Against the backdrop of 3.7 billion years during which microbes have been present on Earth, 1 million years is not a long time in terms of evolution. In the case of Lake Vostok, rates of evolution are likely to slow under the conditions of low temperature and low microbial productivity. The result is likely to be that the metabolically active and growing microorganisms present in these communities should represent those better adapted to the ambient conditions but will still be related to microorganisms found in other environments today.
A much longer time for evolution may have occurred if, however, the original inoculum to Lake Vostok dates back to the time of the isolation of the lake from the overlying atmosphere more than 15 million years before the present. This time of isolation could be even longer if the founding populations were derived from rocks or sediments. In this latter case, the microbial populations could have been isolated from the surface approximately 35 million to 40 million years ago, prior to the formation of the lake.
Samples of microbes from water and sediment are the only way to answer these questions of the uniqueness of microbial life in subglacial aquatic systems. Although the effect of the extreme conditions is unknown, there is a chance that the microbes have been isolated long enough that significant genetic divergence of microbial lineages has occurred.