Methane trapped in the 3,053-m-deep Greenland Ice Sheet Project 2 ice core provides an important record of millennial-scale climate change over the last 110,000 yr. However, at several depths in the lowest 90 m of the ice core, the methane concentration is up to an order of magnitude higher than at other depths. At those depths we have discovered methanogenic archaea, the in situ metabolism of which accounts for the excess methane. The total concentration of all types of microbes we measured with direct counts of Syto-23-stained cells tracks the excess of methanogens that we identified by their F420 autofluorescence and provides independent evidence for anomalous layers. The metabolic rate we estimated for microbes at those depths is consistent with the Arrhenius relation for rates found earlier for microbes imprisoned in rock, sediment, and ice. It is roughly the same as the rate of spontaneous macromolecular damage inferred from laboratory data, suggesting that microbes imprisoned in ice expend metabolic energy mainly to repair damage to DNA and amino acids rather than to grow. Equating the loss rate of methane recently discovered in the Martian atmosphere to the production rate by possible methanogens, we estimate that a possible Martian habitat would be at a temperature of ≈0°C and that the concentration, if uniformly distributed in a 10-m-thick layer, would be ≈1 cell per ml.
Keywords: metabolism by methanogenic archaea, methane in glacial ice, methanogens on Mars, origin of microbes in glacial ice
The record of atmospheric methane (CH4) concentration trapped in the Greenland Ice Sheet Project 2 (GISP2) ice core serves as a climate proxy, showing that climate during the last glacial period oscillated rapidly between cold and warm states that lasted for several thousand years (1). The source is believed to be wetland methane emissions that depend on temperature, precipitation, net ecosystem production, and oxidation by tropospheric OH. Because of its short atmospheric mixing time relative to its lifetime, variations of methane recorded in ice cores are believed to reflect global changes in the methane budget.
Fig. 1 shows measurements of methane in the GISP2 ice core as a function of depth by Ed Brook [National Oceanic and Atmospheric Administration Geophysical Data Center (www.ngdc.noaa.gov/paleo/paleo.html); and E. Brook, additional data for depths of 2,806–3,038 m, personal communication] down to 3,038 m, just 3 m above the silt-laden basal ice. All but four of his methane values range between 337 and 880 parts per billion by volume (ppbV) and correlate with other climate proxies such as δ18O and CO2 (1). The intervals between his samples were >10 m at depths Fig. 1, which stand out above the 99% that are related to climate. We report here our discovery that the excess methane values are produced by methanogens (microbes that metabolize with emission of methane) that were metabolizing while frozen within the ice at those depths. We also show that their average in situ metabolic rates correspond to a cellular carbon turnover time of ≈105 yr at an ice temperature of –11°C.
Bacteria and archaea have been found in all subfreezing terrestrial environments (2–6). Studies of terrestrial psychrophiles and psychrotrophs have involved extraction and examination of cells from cold water, ice, or permafrost. Studies of microbial life in cold environments on Earth help us to understand how life could have arisen on cold planets such as Mars. Instruments to look for chemical evidence of extant or extinct life in the Martian subsurface are being developed for future missions, and Mars samples eventually will be returned to Earth for study. Ideally, remote selection of such samples can be expedited by equipping rovers with instruments that exploit molecular signatures of microbial life rather than just by photography of Martian surface morphology or rock type.
Hints of microbial production of excess greenhouse gases in glacial ice have been reported. In a study of N2O in portions of the Vostok ice core, Sowers (7) found a 30% excess at a depth corresponding to the penultimate glacial maximum [≈135,000 yr (135 kyr) ago], at which excess bacterial counts and dust had been found, and he suggested that the N2O had been produced in situ by nitrifying bacteria. Flückiger et al. (8, 9) reported occasional spikes of excess N2O at several depths in the Greenland Ice Core Project (GRIP) and North GRIP ice cores and referred to them as N2O “artifacts.” They found no spikes of excess CH4 at those depths. Flückiger listed microbial activity in glacial ice as one of four possible explanations for the N2O artifacts (10). Campen et al. (11) reported very large excesses of CO2, CH4, and N2O (≈32, 8, and up to 240 times greater than the tropospheric values, respectively) at two depths in air extracted from the Sajama (Bolivia) glacier. They concluded that the best explanation for the excesses of these gases was that they were products of in situ microbial metabolism. None of the authors noted above searched for microbes in their ice samples.
Since those studies, following up on a report of huge excesses of CO2 and CH4 in silt-laden basal ice at the GRIP site (12), two groups discovered very high concentrations of microbes in silt-laden basal ice at the nearby GISP2 site (5, 6, 13, 14). Price and Sowers (13) measured both CH4 and microbial concentrations in the GISP2 basal ice and concluded that in situ metabolism at –9°C accounted quantitatively for the excess CH4. The silty, basal ice probably originated in flow-induced mixing of glacial ice with a frozen wetland soil (12) some 3 × 105 yr ago (14).
Source: Proc Natl Acad Sci U S A. 2005 December 20; 102(51): 18292–18296. Copyright © 2005, The National Academy of Sciences