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Vol. 97, Issue 3, 1247-1251, February 1, 2000
Physics Department, University of California, Berkeley, CA 94720
Contributed by P. Buford Price, November 29, 1999
Microbes, some of which may be viable, have been found in ice cores
drilled at Vostok Station at depths down to It seems to be a fundamental
law that, wherever microbial life can survive, it will be found to
exist (1). Microbes are amazingly hardy; viable specimens of a
spore-forming bacillus and of an extremely halophilic bacterium have
been found in an inclusion in a 250-million-year-old salt
crystal. Evidence for Microbial Life in Deep Antarctic Glacial Ice.
Consider first airborne sources of microbes blown onto snow and
compacted into the polar ice. Working with filtered (0.2 µm), melted
ice from depths down to 2,750 m in the ice core from Vostok Station
(east Antarctica), Abyzov et al. (9) studied the
concentration and morphology of microbes stained with a fluorescent
dye. Concentrations as a function of depth (and thus of age) ranged
from
Geophysics / Microbiology
A habitat for psychrophiles in deep Antarctic ice
Abstract
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Abstract
Article
References
3,600 m, close to the
surface of the huge subglacial Lake Vostok. Two types of ice have been
found. The upper 3,500 m comprises glacial ice containing traces of
nutrients of aeolian origin including sulfuric acid, nitric acid,
methanosulfonic acid (MSA), formic acid, sea salts, and mineral grains.
Ice below 3,500 m comprises refrozen water from Lake Vostok,
accreted to the bottom of the glacial ice. Nutrients in the accretion
ice include salts and dissolved organic carbon. There is great interest
in searching for living microbes and especially for new species in
deepest Antarctic ice. I propose a habitat consisting of interconnected
liquid veins along three-grain boundaries in ice in which psychrophilic
bacteria can move and obtain energy and carbon from ions in solution.
In the accretion ice, with an age of a few 104 years and a
temperature a few degrees below freezing, the carbon and energy sources
in the veins can maintain significant numbers of cells per cubic
centimeter that are metabolizing but not multiplying. In the 4 × 105-year-old colder glacial ice, at least 1 cell per
cm3 in acid veins can be maintained. With fluorescence
microscopy tuned to detect NADH in live organisms, motile bacteria
could be detected by direct scanning of the veins in ice samples.
Article
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Abstract
Article
References
A
bacterial spore has been revived, cultured, and identified from
40-million-year-old amber (2). Microbial life has been found at depths
down to several kilometers in the earth's crust (3), and viable
bacterial populations have been discovered at Pacific Ocean sites to
depths of >500 m in sediments (4). Bacteria can grow and reproduce at
temperatures 
0°C in high-altitude cloud droplets (5). Microbial
communities survive on wind-deposited sediment particles within liquid
water inclusions in permanently ice-covered Antarctic lakes (6). Before
Antarctica developed its permanent ice cap some 14 million years ago
(7), microbes may well have existed in its continental crust, and their
descendants may live in subglacial rock crevices, lakes, and sediments
and perhaps even in the glacial ice itself. Far less is known about psychrophilic (cold-loving) bacteria than about thermophiles, and it is
not even certain yet whether life on earth originated in a hot or cold
environment (8). It seems worthwhile to devise an in situ
search for live microorganisms in ancient polar ice. In this paper, I
propose a habitat that will sustain a small population of psychrophilic
bacteria in deep Antarctic ice in the absence of sunlight or oxygen, at
pressures up to 400 bars (1 bar = 100 kPa), at temperatures well
below 0°C, and in strongly acidic or saline solutions.
103 to 104 cells
per cm3 and correlated with dust concentration,
which suggests that they were deposited in the snow preferentially
during glacial periods when the flux of dust and the wind speed were
greatest. In addition, the authors used consumption of a
14C-labeled protein hydrolysate as a crude
measure of cell viability. Superimposed on a general decline of
radiocarbon uptake as a function of depth of origin of the sample (from
0.0044 µg per liter per h at 1,665 m to 0.0002 µg per liter per h
at 2,750 m), they found a very low uptake in cells from depths
corresponding to cold periods.
650
m deep at the deepest end and has a density consistent with that of
fresh water. Workshops in St. Petersburg, Russia (13), Washington,
DC
, and
Cambridge,
England§, were
devoted to discussions of prospects for drilling into the lake. At the
St. Petersburg workshop, Petit (14) reported that the bottom 100 m
of a 3,623-m-deep Vostok ice core that reached a depth 120 m above
the lake consists of refrozen lake water, called "accretion ice,"
whose crystals range in size from 0.1 to 1 m. The accretion ice
is believed to extend another 100 m from the bottom of the core to
the lake surface. Ionic composition measurements and dc electrical
conductivity measurements (see Table 1)
have since shown that the accretion ice seems not to be acidic,
presumably reflecting the composition of the lake water. At the
Cambridge workshop, Priscu et al. (14) reported detection in
melted accretion ice of 3 × 103 to 4 × 104 bacterial cells per ml, which were not
culturable and did not incorporate radiocarbon during 52 h in air
at 1 bar. Karl et al. (15) also reported evidence for
microbial life in their sample of melted accretion ice: the presence of
dissolved organic carbon (7 µM), including 100 pg/liter of
lipopolysaccharides, and sluggish uptake of
14CO2 into biomolecules. A
small fraction of the microbes in the accretion ice is viable but
probably not capable of reproducing. In contrast to the atmospherically
deposited microbial life found at depths down to 2,750 m in the Vostok
ice core (9), life in Lake Vostok might have emerged from sediments,
from cracks in bedrock, or even from thermal vents and might have
migrated upward into the accretion ice. Without direct measurements,
this hypothesis is only speculation. No one has yet observed living, motile organisms in situ in unmelted glacial freshwater ice.
|
Liquid Veins in Vostok Ice.
Fig. 1 shows a habitat that I argue can
provide microbes in polar ice with the three ingredients essential for
life: water, energy, and carbon. The high dc electrical conductivity of
cold polar ice had long provided indirect evidence for aqueous acid solutions concentrated in veins (16). Aqueous veins at the linear junctions of three ice crystals in temperate glaciers are now known to
form a continuous network, and laboratory experiments have clarified
their geometry (17). Using a scanning electron microscope equipped with
a cold stage and an energy-dispersive x-ray microanalyzer, Wolff
and coworkers (18, 19) showed that sulfur was concentrated
in veins and was undetectable in the bulk of the ice. They estimated
that, in a region where a vein roughly 1 µm2 in
cross section intersected the surface of an ice sample, the concentration of sulfuric acid was about 2.5 M. From the mean crystal
size of their sample, they estimated that the melt water concentration
of acid was 7 µM and thus that most, and perhaps all, of the acid
was concentrated in veins. They later showed that hydrochloric acid can
also concentrate in veins (20). Recently, using a micrometer-size laser
beam, Fukazawa et al. (21) inferred from Raman spectra that
aqueous solutions of sulfuric and nitric acid are concentrated in veins
in Antarctic ice as HSO4
and NO3 ions. The
evidence is thus strong that all three of the major mineral acids do
collect in veins.
|
73°C), hydrochloric acid (88°C), nitric acid (43°C), MSA (75°C), and formic
acid (49°C), are low enough to ensure that, in thermodynamic
equilibrium, they will exist as liquids in veins within solid pure ice.
It seems unlikely, however, that solid salt grains intersected by a
grain boundary will end up in aqueous solution in veins, and certainly
mineral dust grains will not.
To develop a quantitative model, consider ice at temperature
T in which an aqueous solution of acids and other soluble
impurities is entirely located in veins of uniform radius
rvein, where
rvein is the radius of an equivalent
cylinder (not the radius of curvature of the vein interface, which is
convex inwards). In accordance with the work of Frank (22), I model
polycrystalline ice as consisting of grains of semiregular truncated
octahedra of diameter (between square faces) D. The volume
of a grain is D3/2, and it has 36 edges, each of length 
2D/4, each shared with three
other grains. The total fractional volume
(f) in veins is
|
[ 1 ] |
|
[ 2 ] |
ice = 0.915 g/cm3. Cvein
is determined by the free-energy requirement that, in equilibrium, the
two-phase system (i.e., pure ice + aqueous solution) be on the freezing
line of its phase diagram. Thus, Cvein
is a function of ice temperature that can be found by judicious use of
tables that give the depression of the freezing point as a function of
concentration for various solutions (23). Once
Cvein is known, vein diameter is found
from
|
[ 3 ] |
Ionic Composition.
Table 1 shows the data from which the molarity in veins and the vein
diameter were calculated as a function of temperature of Vostok ice.
The bulk concentrations of ions in Vostok ice at a depth of 3,300 m
(corresponding to an age of 4 × 105
years) were taken from unpublished tables provided by M. Legrand (personal communication; see also ref. 24), and the concentrations for
accretion ice were provided by Priscu et al. (14) and Karl et al. (15). The ionic activities of each of the ion species contribute additively to depression of the freezing point (23, 25). The
balance of positive ions in the ancient ice is provided by
H+ (26), whereas the composition of the accretion
ice seems to be accounted for by salts and not to require
H+ ions.
Composition and Size of Veins.
Fig. 2 shows results for ancient Vostok
ice, and Fig. 3 shows results for
accretion ice. The accretion ice extends from 3,538 m to the lake
surface at 3,750 m, and the Vostok core retrieved ice down to a
depth of 3,623 m. From 3,538 to 3,608 m, the ice contained numerous mud
inclusions 1 mm in diameter, presumably incorporated from materials
along the lake margin. Below 3,608 m, the ice is very clear and is
thought to have accreted from freezing of lake water to the base of the
ice sheet as it passed over the lake. The temperature gradient in the
lowest few hundred meters of ice is taken to be 0.02°C/m. The
abscissae in Figs. 2 and 3 give freezing point depression relative to
the pressure melting point, found from the relation dT/dP = 0.0074°C/bar to be 2.8°C for pure ice just above the lake
surface. The mean grain size of the glacial ice was taken to be
D = 2 cm, and that of accretion ice was taken to be
D = 30 cm (13). Because vein diameter scales linearly
with D, it is easy to find
dvein for other choices of
D. The main difference between the two environments, other than differences in impurity concentrations and differences in grain
size, is that ancient ice scavenges only acids, not salts, into veins,
whereas accretion ice freezes from lake water in which all the ions are
dissolved. Figs. 2 and 3 show that, at temperatures down to a few
degrees below the pressure melting point, vein diameter is easily large
enough to accommodate motile micrometer-size bacteria. With decreasing
depth, the temperature decreases, reaching 56°C at the surface, and
the vein diameter decreases to a few micrometers, with a concomitant
increase in molarity of the acids.
|
|
Energy Source. For bacteria in veins, aqueous sulfuric acid and nitric acid are the main electron acceptors. MSA (HCH3SO3), formic acid (HCOOH), and acetic acid (CH3COOH) will also be swept into veins and will provide energy and carbon for biosynthesis. Dissolved organic carbon is present in Vostok ice (Table 1), but its composition and location are not known.
I have shown that segregation of acids into veins raises the concentrations of nutrients and of dissolved carbon as much as a million-fold, depending on ice temperature and crystal size, thus providing channels of aqueous solution in which microorganisms can live and extract energy. For those microbes that find themselves in veins, maintenance of life seems likely, given the demonstrated adaptability of life to extreme environments. Eqs. 4 and 5 provide examples of reactions that provide both energy and carbon: decomposition of MSA at a concentration of0.1 M in ancient ice (Eq. 4) and formic acid at a lower composition together with
sulfuric acid (Eq. 5). The substantial changes in
standard-state Gibbs free energy, 
G°, shown under each
equation are essentially independent of temperature and concentration
in the ranges of interest. Formic + nitric acid would also work.
Formate is interesting, because some bacteria are known to sense and
move toward formate under anaerobic conditions.
|
[ 4 ] |
G° = 55 to 56 kcal/mol at 10 to 40°C)
|
[ 5 ] |
G° = 84.5 to 81 kcal/mol at 10 to 40°C)
Hyperacidophiles are known (27-29) that can exist at pH
0. A fungus, Acontium velatum, has been cultured in 2.5 M
H2SO4 (30). Thiobacillus-like bacteria are able to grow (27, 28) both at
very low pH and at temperatures below 0°C in a mine in Greenland at
83°N. To survive in veins in the deep ice, the microbes depicted in
Fig. 1 must be able to withstand temperatures below 0°C, without oxygen, in the dark, and at pressures up to 400 bars. In addition, those in strongly acidic veins must consume energy to operate a strong
proton pump or have a low proton membrane permeability to maintain
their interior at nearly neutral pH. Those in accretion ice at
subfreezing temperature will have to tolerate salt at 1 to 2 M.
Carbon Supply Limits Population Size.
The age of the glacial ice at 3,300 m in the Vostok core is
4 × 105 years. A freezing rate of
several millimeters to several centimeters per
year
for the accretion ice implies that it is
much younger, reaching only a few 104 years at
100 m above Lake Vostok. Assuming that the source of energy and
carbon is MSA and taking a bulk molarity of 0.084 µM for MSA in
liquid veins, I use data from refs. 5 and 31 to estimate the bacterial
population size that could be maintained for times of 4 × 105 years in glacial ice and for
104 years in accretion ice. I assume that
microbes in veins in ice have a composition
CH1.8O0.5N0.2,
a cell volume of 0.084 µm3, and a dry mass of
30 fg (5).
3 × 105 g of carbon per g of biomass carbon per h
at 15°C was needed to prevent microbial carbon loss during
incubation. (This amount is about 1/1,000 of that typically consumed
by biomass in laboratory cultures.) Then, for 4 × 105 years, the MSA in glacial ice would maintain
a population per cubic centimeter of ice of approximately seven cells
that are biologically functional but not multiplying. In
104-year-old accretion ice, more than
102 cells per cm3 would be
found. Because the ice temperature is at least 20°C colder than that
of the biomass studied by Morita, the lower metabolism rate in ice
would permit an even larger population to survive.
In their study of bacteria collected from supercooled cloud droplets,
Sattler et al. (5) measured an uptake rate at 0°C of
2 × 1021 mol thymidine
h1 per cell, a rough measure of cell growth.
Equating MSA to thymidine as a source of carbon, the thymidine uptake
rate leads to estimates of 10 and 400 cells per
cm3 for the sustainable populations of bacteria
in ice of ages 4 × 105 and
104 years, respectively. These estimates are very
similar to those based on Morita's data.
If the dissolved organic carbon listed in Table 1 can also be
incorporated into cells, a still larger population could be maintained.
Searching for Living Bacteria in Veins.
By exploiting their confinement to liquid veins, one could easily
search for bacteria in situ. In collecting an ice core from great depth where the ice is relatively warm, it would be desirable to
preserve bacteria in the veins in an anaerobic and thermal environment
similar to that to which they were acclimated. Because vein size in
equilibrium depends on ice temperature, one would have to maintain the
ice samples at a roughly constant temperature during shipping and
study. In ancient ice with D = 2 cm, the length of vein
that would have to be scanned for bacterial cells would be only 2 cm
per cm3 of ice. It would be easy to scan 10 cm3 or more in a low-power microscope by using
phase contrast or fluorescence microscopy. In principle, one could
introduce a dye specific to certain molecules into liquid veins. Saito
(32) has shown that 8-anilinonaphthalene 1-sulfonate will indicate the
presence of cells; sulfofluorescein diacetate can be used to detect
certain enzymes such as esterase; and ethidium bromide can
identify nucleic acids. It would be easier, however, to avoid dyes by
using 366-nm light to search for NADH, which marks the existence of a
living cell by fluorescing at 440 nm
(33).¶ With
103 to 106 NADH molecules
per living cell, the signal from a single cell would be strong. In a
dead cell, NADH is oxidized to NAD, which does not fluoresce.
A Subglacial Lake at the South Pole. In their analysis of airborne radar surveys of Antarctica, Siegert et al. (34) found evidence for at least 77 subglacial lakes, one of which has subsequently proved to be only a few kilometers from the South Pole Station (D. Blankenship and D. Morse, unpublished results). The idea of collecting water, ice, and sediments from the South Pole subglacial lake has both advantages and disadvantages compared with sampling Lake Vostok. Being only a few kilometers in size, the South Pole lake and the surrounding bedrock would be easy to characterize by radar mapping and seismic sounding, and being close to the infrastructure of the South Pole Station, researchers would have easy access to modern laboratory facilities for study of samples to be recovered by sterile drilling techniques. One could, for example, use a pressure-resistant waterproof fluorescent camera for assaying ice for living cells as a drill is being lowered toward the lake.
Greenland Glacial Ice.
No subglacial lakes exist in Greenland. Two cores have been
drilled to bedrock at Dome Summit, Greenland
(35).
The grain
size reaches 2-3 cm in the bottom 80 m, at depths below 2,950 m.
The temperature and age near bedrock are 9°C and 250,000 years, respectively. The impurities in Dome Summit ice are generally not acidic (unlike Vostok ice), and there is somewhat more formate and
acetate than at Vostok. dc electrical measurements show that the
conductivity (a measure of [H+] and of
conducting veins) is much lower than that in Antarctic ice. It thus
seems unlikely that there is a network of liquid veins hospitable to
psychrophiles in these cores.
Concluding Comments.
The liquid vein habitat provides microbes with intimate access to
water, energy, and carbon. By contrast, metabolism of microbes encased
in solid ice must overcome a seemingly insuperable barrier: diffusion
of nutrients through a solid is orders of magnitude slower than it is
through a liquid. The advantages of scanning liquid veins in solid ice
with fluorescence microscopy are that contamination would be ruled out,
that living microbes could be distinguished from dead ones, and that a
concentration of as low as 1 cell per cm3 could
be detected in veins, despite a high background of dead matter not
located in veins. We do not yet know of any species capable of
tolerating all of the following conditions: no sunlight, no
oxygen, pressure of 400 bars, temperature below 0°C, and a highly
acidic or saline medium. It is thus likely that microbes living in
liquid veins in ancient ice would be different from any yet known.
Another interesting outcome of a search for living microbes in liquid
veins in ice of known age would be to determine from the population
density whether oligotrophic psychrophiles have developed an unusually
high metabolic efficiency that permits long-term survival on very
limited extracellular energy resources.
| |
Acknowledgements |
|---|
I am indebted to Sridhar Anandakrishnan, Don Blankenship, Frank Carsey, Michael Goldfeld, Michel Legrand, Donal Manahan, Rollie Myers, Ken Nealson, Norm Pace, Linda Powers, John Priscu, Roland Psenner, Takeshi Saito, Jose de la Torre, and Eric Wolff for discussions. This work was supported in part by National Science Foundation Grant PHY-9971390.
| |
Abbreviation |
|---|
MSA, methanosulfonic acid.
| |
Footnotes |
|---|
* To whom reprint requests should be addressed. E-mail: bprice{at}uclink4.berkeley.edu.
Vreeland, R. H., Vay, H., Bartell,
J. H. & Rosenzweig, W. D. American Society for Microbiology,
99th General Meeting, June 2, 1999, Chicago.
Bell, R. & Karl, D., Proceedings of the Lake
Vostok Workshop: A Curiosity or a Focus for Interdisciplinary Study?,
Nov. 7 and 8, 1998, Washington, DC.
§ Ellis-Evans, C., Proceedings of the Workshop on the Exploration of Antarctic Subglacial Lakes, Sept. 25-27, 1999, Cambridge, England.
¶ Powers, L. & Ellis, W., Jr., Defense Advanced Research Projects Agency. Conference on Biological Agent Detection and Identification, April 27-30, 1999, Washington, DC.
See ref. 35 for 47 papers devoted to
research on the two deep ice cores drilled in central Greenland during
1989-1993 by the U.S. Greenland Ice Sheet Project 2 and the European
Greenland Ice Core Program.
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B. C. Christner Incorporation of DNA and Protein Precursors into Macromolecules by Bacteria at -15oC Appl. Envir. Microbiol., December 1, 2002; 68(12): 6435 - 6438. [Abstract] [Full Text] [PDF]
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P. B. Price, O. V. Nagornov, R. Bay, D. Chirkin, Y. He, P. Miocinovic, A. Richards, K. Woschnagg, B. Koci, and V. Zagorodnov Temperature profile for glacial ice at the South Pole: Implications for life in a nearby subglacial lake PNAS, June 11, 2002; 99(12): 7844 - 7847. [Abstract] [Full Text] [PDF]
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N. R. Pace Special Feature: The universal nature of biochemistry PNAS, January 30, 2001; 98(3): 805 - 808. [Full Text] [PDF]
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