PNAS | February 27, 2001 | vol. 98 | no. 5 | 2148-2153
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Special Feature
Geology
Oxygen isotope ratios of PO4: An inorganic indicator
of enzymatic activity and P metabolism and a new biomarker in the
search for life
Ruth E.
Blake*,
,
Jeffrey C.
Alt
, and
Anna M.
Martini§
* Department of Geology and Geophysics, Yale University, New Haven,
CT 06520-8109; Department of Geology, University of
Michigan, Ann Arbor, MI 48109; and § Department of
Geology, Amherst College, Amherst, MA 01002
Edited by Karl K. Turekian, Yale University, New Haven, CT, and
approved December 29, 2000 (received for review October 29, 2000)
 |
Abstract |
The distinctive relations between biological activity and isotopic
effect recorded in biomarkers (e.g., carbon and sulfur isotope ratios)
have allowed scientists to suggest that life originated on this planet
nearly 3.8 billion years ago. The existence of life on other planets
may be similarly identified by geochemical biomarkers, including the
oxygen isotope ratio of phosphate (
18Op)
presented here. At low near-surface temperatures, the exchange of
oxygen isotopes between phosphate and water requires enzymatic catalysis. Because enzymes are indicative of cellular activity, the
demonstration of enzyme-catalyzed PO4-H2O
exchange is indicative of the presence of life. Results of laboratory
experiments are presented that clearly show that
18OP values of inorganic phosphate can be
used to detect enzymatic activity and microbial metabolism of
phosphate. Applications of 18Op as a
biomarker are presented for two Earth environments relevant to the
search for extraterrestrial life: a shallow groundwater reservoir and a
marine hydrothermal vent system. With the development of in
situ analytical techniques and future planned sample return strategies, 18Op may provide an important
biosignature of the presence of life in extraterrestrial systems such
as that on Mars.
| |
Introduction |
The basic ingredients
required for life include a source of chemical building blocks, energy,
and liquid water (1). Mars has possessed all of these attributes in its
history and may even have extensive reservoirs of subsurface liquid
water today (2, 3). Phosphorus is essential to life on Earth and,
therefore, an obvious candidate for a chemical tracer of the presence
of life in extraterrestrial systems. Results from recent Mars
Pathfinder surveys show relatively high concentrations of P (
0.4 wt
% P2O5) in Mars surface
sediments that are thought to be derived from dissolution of apatite by
aqueous fluids percolating through the surface layers of Mars and later
enriched by evaporation.¶ It has been suggested that
anomalies in phosphorus concentrations and P/Th ratios in sediments
might be useful tracers of extinct life on Mars (4). The occurrence of
phosphate, particularly in association with organic carbon, has been
interpreted as the remains of once living organisms in ancient
sedimentary strata (5, 6). Here, we demonstrate that the unique
chemical and isotopic properties of PO4 make
oxygen isotope ratios of phosphate (18OP) an ideal
signature of the presence of enzymatic activity and, thus, life.
Stable isotope ratios can provide diagnostic signatures of biological
activity because of the large and characteristic isotopic fractionations associated with many metabolic reactions (e.g., bacterial sulfate reduction and photosynthesis). As a result, the
systematics of stable isotope fractionation for key bioelements (C, N,
and S) have been studied extensively, and the isotopic ratios of these
elements have been widely used as biosignatures in both terrestrial and
extraterrestrial samples. An analogous isotopic biomarker system is not
available for P, because, unlike C, N, and S, it has only one stable
isotope. Phosphorus is also distinct from other major bioelements in
that it occurs primarily in one oxidation state (+5), and in one major
form, orthophosphate (PO4).
18OP values have been
used primarily as a paleotemperature proxy recorded in biogenic apatite
minerals found in teeth, bones, fish scales, and shells (7). The
PO4 radical is fairly inert to chemical redox
reactions and to oxygen isotope exchange at low temperature (<80°C).
Enzymes are required for catalysis of oxygen isotope exchange
between PO4 and water at low temperature. They
are often invoked as the cause of diagenetic alteration of phosphate
minerals leading to the loss of integrity of original
18OP values. Detailed
studies of enzyme-catalyzed
PO4-H2O exchange reactions
(8-10) demonstrate that one can exploit this feature to assess
18OP values in a
fundamentally different way: as an indicator of the presence of
enzymatic activity and, hence, living organisms. Few investigators have
examined oxygen isotope compositions of dissolved phosphate and
nonbiogenic phosphate in modern sediments/soils, and, to our
knowledge, no one has attempted to make use of the unique dependence of
PO4-H2O oxygen isotope
exchange on enzyme activity specifically as a biomarker. Here, we
demonstrate the application of
18Op as a biomarker in
two terrestrial systems that serve as analogues for extraterrestrial
planetary environments highly targeted in the search for life: a
groundwater aquifer, and a marine hydrothermal vent system. Continued
advances toward in situ sampling and analytical techniques,
as well as sample-return missions planned for Mars, make
18O analysis of phosphate and water in
extraterrestrial materials plausible in the near future.
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Method Development |
Analytical Methods.
Oxygen isotope ratios of PO4 reported in this
study were determined by conversion of inorganic
PO4 extracted from groundwater or sediments into
silver phosphate. The silver phosphate was then converted to
CO2 after the method of O'Neil et al.
(11) or by conventional fluorination by using
ClF3. Water samples were analyzed by the standard
method of CO2-H2O
equilibration (12). Isotopic analyses were carried out in the stable
isotope facilities at the University of Michigan (ISOLAB) and Yale
University. Precision of the isotopic analyses was ±0.1
(1
) for
water and ±0.2 for phosphate.
All oxygen isotope data are reported in the standard delta notation in
per mil () relative to the SMOW (standard mean ocean water)
international reference standard. The fractionation factor, 
,
between PO4 (p) and water (w) is defined as
p-w = (1 + 18OP/1,000)/(1 + 18OW/1,000).
Microbial growth and phosphate metabolism studies were carried out as
described in the legends of associated figures and data tables.
Calibration of the 18OP Biomarker.
To employ this potential biomarker, we must first consider the
processes recorded by inorganic PO4 dissolved in
natural waters and associated with sediments. Reactions of
PO4 in natural waters, sediments, and soils are
largely under biological control because of the importance of P as a
nutrient for microorganisms and plants. There are very few studies of
the oxygen isotope systematics of dissolved PO4
and P cycling in natural waters and sediments (13, 
). However, oxygen isotope
compositions of PO4 precipitated by living
organisms in the form of biogenic apatite minerals (teeth, shells, and
bone) have been studied extensively (e.g., refs. 14-16). Biogenic
phosphate is equilibrated with body fluids of an organism as a result
of intracellular enzymatic reactions (e.g., ATP utilization and
phosphorylation/dephosphorylation). The temperature dependence of
oxygen isotope fractionation between apatite and water has been
determined both empirically and in laboratory experiments (17-20). The
most widely cited relation is the empirical equation of Longinelli and
Nuti, t (°C) = 111.4 
4.3[18OP 18OW], which is
generally assumed to reflect equilibrium isotopic fractionation (17).
In contrast to biogenic phosphates, where the exchange of
PO4 with body fluids and subsequent precipitation
as apatite occur in a closed system, the metabolism of P in natural
waters is mediated largely by microorganisms in a relatively open
system. This phenomenon occurs because microbial metabolism of P
compounds (inorganic and organic) involves the action of extracellular
phosphate-scavenging enzymes and intracellular-extracellular
PO4 exchange processes (ion transport proteins),
resulting in the release of inorganic PO4 into
the extracellular environment (21). Many of these enzymatic reactions
involving PO4 are dominated by hydrolytic
cleavage reactions that facilitate the incorporation of water (from the
medium) into PO4. These reactions promote
significant PO4-H2O oxygen
isotope exchange that is reflected in the 18O
value of dissolved PO4. Biochemists have
exploited this property for decades in elegant studies of phosphoenzyme
reaction kinetics and mechanisms by using heavily labeled (e.g., >90%
18O) water and P compounds (22, 23). The capacity
of 18OP as a biomarker
at natural 18O abundance levels also results from
its ability to record enzymatic activity, and from the lack of
significant PO4-H2O oxygen isotope exchange by
other abiotic geochemical processes involving P. For example, the
precipitation of dissolved phosphate as apatite, important during
sediment diagenesis, does not involve exchange of
PO4 oxygen isotopes and results in only small
dissolved PO4-apatite fractionations (1; R.E.B. and
Y. Liang, unpublished data).
The low dissolved PO4 concentrations found in
most natural systems, coupled with intense biological recycling and
turnover characteristic of P (24), should ensure complete oxygen
isotope exchange between dissolved PO4 and
ambient water. Thus, oxygen isotope ratios of dissolved
PO4 in natural waters and associated with
sediments should record the effects of microbial P metabolism and
microbial enzyme activity at the ambient environmental water and
temperature conditions.
In summary, 18OP values
can be used to detect enzymatic activity in two ways: (i) by
recording exchange between PO4 and ambient water,
and (ii) by recording ambient temperature. Both result from
the process of PO4-H2O
oxygen isotope exchange. At low near-surface temperatures,
PO4-H2O exchange is
catalyzed by the action of enzymes. Results from detailed laboratory
studies of oxygen isotope fractionation associated with microbial
metabolism of P compounds and enzyme catalyzed
PO4-H2O exchange reactions
provide a context for the interpretation of
18OP values and for the
detection of enzymatic activity in natural systems.
Relation between 18OP,
18OW, and Temperature.
Extensive oxygen isotope exchange between water and dissolved
PO4 is demonstrated in laboratory experiments
where bioavailable P compounds (inorganic orthophosphate and organic
phosphoesters) were metabolized by microorganisms (Fig.
1; Table 1)
or degraded by purified cell-free phosphoenzymes (Fig.
2; Table 2;
refs. 8 and 9). This exchange occurs even at dissolved PO4
concentrations that are more than 1,000 times those typical of natural
systems. Phosphate-water exchange is reflected in a strong positive
correlation between the 18O value of water and
the 18O value of dissolved PO4 (Figs. 1 and
2). Experiments with bacteria also show that microbial metabolism of P
is characterized by equilibrium oxygen isotope fractionations that vary
with temperature in a manner similar to that observed for biogenic
apatites (Fig. 3; Table
3). Similar results were obtained
in experiments on the temperature dependence of
PO4-H2O oxygen-isotope
exchange catalyzed by cell-free, purified enzymes (R.E.B., J. R. O'Neil, and G. A. Garcia, unpublished data), demonstrating that
catalytic molecules that are derived from, or possibly precursors of,
complex cells may also leave behind a distinctive geochemical signature
of biological activity.
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Fig. 1.
Microbial P metabolism experiments. Mixed (from soils, rivers) and pure
strains of microorganisms [e.g., Klebsiella, Bacillus,
Aquaspirillum) were grown on representative bioavailable P
compounds (inorganic orthophosphate (Pi), organic P
monoesters (glucose-PO4) and diesters (RNA)] to study
PO4-H2O oxygen isotope exchange during
microbial metabolism of P. Microbial metabolism of P leads to a
positive correlation between 18O of water and
18O of dissolved PO4 in the medium, for both
inorganic and organic P substrates. Plots show representative data from
25°C and include data from Blake et al. (8, 9).
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Table 1.
Oxygen isotope compositions of water and dissolved
inorganic PO4 derived from various P sources and
metabolized by microbial cell cultures at 25°C and plotted in Fig.
1
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Fig. 2.
Purified cell-free enzyme catalyzed
PO4-H2O oxygen isotope exchange. Positive
correlation between 18O of dissolved inorganic
PO4 and water resulting from
PO4-H2O exchange catalyzed by hydrolytic
phosphoenzymes inorganic pyrophosphatase (PPiase) and alkaline
phosphatase (APase). (a) PPiase exchange experiments at
22°C and 30°C in water with 18O of 19.7 to
96.4. The initial 18Op value of dissolved
inorganic PO4 before exchange was 13.5.
(b) APase exchange experiments in 19.4 and 44.1
water at 37°C using glycero-2-phosphate as an organic-P substrate (P
source).
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Table 2.
Oxygen isotope compositions of water and dissolved
inorganic PO4 derived from reaction of organic-P compounds
and inorganic PO4 with purified, cell-free phosphatase
(hydrolytic)
enzymes
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Fig. 3.
Temperature dependence of PO4-H2O oxygen
isotope exchange accompanying microbial metabolism of P compounds. The
PO4-H2O fractionations produced by bacteria
agree well with fractionations determined from biogenic apatites.
Biogenic apatite data are from Longinelli and Nuti (18) and are the
basis for the PO4-H2O thermometry equation:
t (°C) = 111.4 4.3[18OP 18OW] (18). Microbial phosphate data from
Blake et al. (8, 9).
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Table 3.
Oxygen isotope ratios of water and dissolved inorganic
phosphate liberated during microbial degradation of organophosphorus
compounds (RNA) at 20 to 35°C
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The above results indicate that microbial metabolism of P should
result in oxygen isotope exchange between dissolved
PO4 and ambient water, regardless of the nature
(organic or inorganic) or initial 18O value of
the P source. Further, such metabolized PO4
should record the temperature of equilibrium exchange according to the same relation used for oxygen isotope thermometry of biogenic apatites.
Therefore, in conjunction with measured or inferred temperature and
18Ow values, the
18O value of dissolved
PO4 and sediment-associated
PO4 can be used to detect enzymatic activity and,
thus, infer the presence of life.
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Application of the  18OP Biomarker |
Dissolved PO4 in Groundwater
Correlation Between
18Ow and 18OP.
Oxygen isotope ratios of dissolved PO4 from a
shallow glacial outwash aquifer in Cape Cod, MA were measured in a
study of microbial turnover of PO4 in
groundwater.¶ Dissolved phosphate concentrations
(30-108 µM) reach levels that are 1 to 2 orders of magnitude higher
than those in typical aquatic and marine systems because of
contamination of the ground water by sewage. Phosphate within the
contaminant plume is not fully equilibrated with ground water at
measured ambient aquifer temperatures (Table
4). Complete metabolic turnover and
exchange of the entire phosphate pool with water is probably limited by
low dissolved organic carbon concentrations in the aquifer. At
dissolved PO4 concentrations more typical of
uncontaminated systems (<5 µM), it is expected that the entire
phosphate pool will be metabolized and more fully equilibrated with
water.
18O values of dissolved
PO4 in the groundwater show clear evidence of
phosphate metabolism. There is a positive correlation between the
18O of water and the
18O of dissolved PO4
(Fig. 4). This correlation suggests that
extensive oxygen isotope exchange has occurred between the water and
dissolved PO4. Importantly, temperatures measured
within the aquifer, approximately 8°C to 14°C, are much too low for
the observed PO4-H2O
exchange to have occurred by abiotic, nonenzymatic reactions.
Therefore, enzymatic activity and metabolism of dissolved inorganic
PO4 in the groundwater is indicated.
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Fig. 4.
Comparison between the 18O of dissolved PO4
and groundwater from the Cape Cod aquifer. Positive correlation between
18OP and 18OW at
low temperature (8°C to 14°C) indicates the presence of enzyme
catalyzed PO4-H2O oxygen isotope exchange and
active microbial metabolism of P within the aquifer.
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18O of Dissolved Inorganic PO4
Associated with Sediments: Fe Oxide Deposits in a Marine Hydrothermal
System.
Currently, it is widely held that life on Earth may have originated in
hydrothermal systems (25). Protected from intense UV irradiation by
overlying water, the first biomolecules and primitive cellular life may
have evolved in deep-sea vent environments by using the energy supplied
by hydrothermal activity and reduced forms of sulfur and hydrogen (25).
Similar hydrothermal systems may have been active over 3 billion years
ago on Mars (26). Phosphate in active and fossil hydrothermal systems
may provide evidence of metabolic activity.
Dissolved inorganic PO4 can become strongly
associated with sediments, especially iron oxides, via sorption or
precipitation processes (27). Hydrothermal iron oxide deposits are
produced by oxidation of erupting hydrothermal fluids rich in reduced
iron, by ambient oxygenated seawater (27, 28) and in some cases, may
involve the action of iron-oxidizing bacteria (29, 30). Iron oxides are
very efficient scavengers and natural concentrators of dissolved
PO4 (27, 31).
The 18OP of
inorganic PO4 associated with Fe oxide deposits
(Fe-PO4) was analyzed from two diffuse flow
hydrothermal systems at Larson's Seamounts located near 21°N along
the East Pacific Rise (EPR) and from Seamount No. 5, located 86 km east
of the EPR near 13°N (refs. 29 and 32, and Table
5). These hydrothermal systems are
located off-axis of the main EPR spreading center. One sampling
site at Red Seamount was experiencing active venting at the time of
sampling whereas the other sites were inactive and comprised fossil
hydrothermal deposits.
Evidence for enzymatic activity and microbial metabolism of the
PO4 associated with these Fe oxide deposits comes
from the temperatures recorded in PO4 oxygen
isotope ratios. Hydrothermal systems provide a variable temperature
structure that can be used to detect
PO4-H2O oxygen isotope
exchange in an otherwise constant 18Ow environment of
ambient seawater. Iron oxides at Red Seamount are believed to have
formed by precipitation from actively venting hydrothermal fluids. At
Green Seamount, the ocherous, Fe oxide sediments are interpreted
to be secondary alteration products formed by oxidation of
iron sulfide minerals precipitated from hydrothermal fluids
(29, 32, 33).
18O values of PO4
associated with iron oxide deposits collected from Red Seamount record
temperatures that are very warm relative to ambient seawater
(2°C-5°C; Table 5). One sample taken from the upper 40 cm of an
actively venting orifice yielded a temperature of 10.8°C that closely
matches measured vent temperatures of 10°C-15°C (29).
18Op temperatures were calculated by using
the PO4-H2O temperature equation (17) and assume a 18O of seawater of
0. The recording of temperatures as low as 10.8°C in
18OP values strongly
suggests that the PO4 has been metabolized and
has undergone oxygen isotope exchange with seawater by enzyme-catalyzed reactions at ambient temperatures.
Temperatures calculated from 18O values of
Fe-PO4 at another site at Red Seamount that was
not actively venting at the time of sampling averaged 60°C. This
higher temperature suggests the venting of warm temperature fluids at
this site in the past. Further evidence for higher temperature
processes in the past at Red Seamount is provided by the presence of
iron-rich talc deposits and from temperatures calculated from
18O values of nontronite deposits (32). A
temperature of 60°C, however, is still too low to promote significant
PO4-H2O oxygen isotope
exchange by inorganic/abiotic means. Thus, the warm temperatures recorded in 18Op values
of these Fe-PO4 deposits also suggest the
presence of enzymatic activity and microbial metabolism of the
PO4.
Oxygen isotope exchange between PO4 and water may
also have occurred deeper within the sediments or in the underlying
basaltic basement rocks at higher temperatures, by the action of
subsurface bacteria. Subsurface vent microbial habitats have been
reported from Loihi Seamount, where thermophilic bacteria with high
metabolic activity were observed at temperatures of 60°C (30).
The mechanism proposed for exchange of
Fe-PO4 with water is microbial uptake and
metabolism of the phosphate. This mechanism requires that
PO4 bound to Fe oxides be biologically available. To assess the bioavailability of Fe oxide-associated
PO4, separate aliquots of the Fe oxide sediments
analyzed for 18Op were
used in microbial growth experiments as a sole source of P. The two
strains of bacteria tested in these experiments, Acinetobacter ADP1 and Shewenella MR-1, were
able to grow readily on minimal media with Fe-PO4
sediments supplied as the sole source of P (Fig.
5). No dissolved
PO4 was detected in the
Fe-PO4 growth media initially or over the course
of the growth experiments, as determined by periodic extraction and
analysis of growth media for dissolved PO4. Under
the oxic conditions of the growth experiments and also of natural
environments of formation of Fe oxides, PO4 is
efficiently scavenged from solution by the Fe oxide sediments.
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Fig. 5.
Bioavailability of PO4 from Red Seamount hydrothermal Fe
oxide deposits. Growth curve measuring changes in optical density of
microbial cultures measured as absorbance at 600 nM, during growth of
Acinetobacter ADP1 on minimal salts medium M9 with
Fe-PO4 sediment as a sole P source at room temperature
(22°C). Fe-PO4 sediments were rinsed with sterile
medium before growth experiments to remove easily desorbed
PO4. No PO4 was released to the rinse buffer
during this procedure.
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18O values of
Fe-PO4 samples from the inactive fossil deposits
at Green Seamount average 25-26 and reflect cold temperatures near
that of the ambient seawater (Table 5). The absence of recorded warm
temperatures in these deposits is also consistent with their mode of
origin as secondary products of the oxidation of hydrothermal iron
sulfides at ambient seawater temperatures.
Iron oxide deposits from both Red and Green Seamount also show
morphological evidence of microbial activity (29, 33). The iron oxides
are composed, almost entirely in some cases, of twisted filaments,
stalks, and hollow sheaths that resemble the characteristic remains of
the iron-oxidizing bacteria Gallionella ferruginea and
Leptothrix known from neutral pH freshwater systems (29).
Similar microbial structures have been observed in iron oxide deposits
from Loihi Seamount (30). High-resolution structural analyses of iron
oxyhydroxides produced by bacteria of the Gallionella and
Leptothrix genus indicate that these iron biominerals have distinct structural orientations (34). Recent discoveries, however, suggest that novel iron-oxidizing bacteria that deposit iron oxides not
in the morphologically distinct stalks and sheaths of
Gallionella and Leptothrix, but as amorphous iron
oxide coatings, may be responsible for the majority of microbial iron
oxidation in near-neutral pH environments such as seawater (35).
Despite strong morphological evidence for the presence of Fe-oxidizing
bacteria in some hydrothermal sediments, the importance of microbial
activity in formation of hydrothermal iron oxides remains the subject
of debate. 18O values of PO4
associated with the microbial iron oxides from Red Seamount provide
independent and strong geochemical evidence of metabolic activity
within these types of sediments. The association of this
PO4 with iron oxides of probable microbial origin
makes Fe-oxidizing bacteria the prime candidate for metabolism of the PO4. The exact location and identity of microbes
responsible for PO4 metabolism in this system is
currently under investigation.
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Implications for the Search for Extraterrestrial Life |
Mounting evidence for the possible existence of liquid water
in subsurface sediments on Mars, beneath the ice-covered surface of
Europa, and most recently, Ganymede and Callisto (36), make application
of the 18OP biomarker tenable. Systems most
likely to be targeted in the search for evidence of extraterrestrial
life are those that show evidence of liquid water today (e.g.,
groundwater seeps on Mars or beneath ice on Europa). In the absence of
water for direct comparison of dissolved PO4
18OP, certain sediment
and mineral phases may be used for
18OP measurement.
Specifically, analyses could be made of sediment-associated PO4 (Fe oxide-bound P) and authigenic phosphate
minerals formed by precipitation of dissolved PO4
from low-temperature fluids, especially occurrences of such phases in
sediments and formations interpreted as lacustrine, fluvial, marine, or
hydrothermal in origin. Any phosphate that has been processed by
biological activity should have an anomalous
18OP value when compared
with 18OP of potential
PO4 sources, such as basaltic Martian bedrock.
On Earth, the largest occurrence of biogenic and biologically
processed PO4 is in marine systems (e.g.,
phosphorite deposits, marine sediments, and dissolved oceanic P).
Compared with high-temperature basaltic and igneous sources of
PO4 (5.3 to 8; refs. 13 and 37), the
18OP of biogenic marine
phosphate has a distinctly heavy signature (20-25; refs. 13
and 17) because of the constant, relatively heavy 18O
value of seawater coupled with the large oxygen isotope fractionations between PO4 and water at low, near-surface
temperatures (Fig. 3). Markel (13) identified biological cycling of
phosphate in lake sediments based solely on varying
18OP values of detrital
and authigenic apatite mineral phases in the sediments, without
requiring the 18O value of the water.
Anomalous 18OP values in
soils have also been attributed to biological activity (37, 38). Thus,
18OP variations and
anomalies in sedimentary and authigenic phosphate phases formed at low
temperature are also indicative of biological activity. The relatively
high concentrations of P measured in Mars surface sediments by Mars
Pathfinder (4),¶ if present as PO4, would
easily allow 18OP analysis.
| |
Conclusions |
It has been suggested that life may exist elsewhere in our solar
system, in near-surface groundwater on Mars (2) or beneath the
ice-covered surface of Europa (39). It is also possible that life
evolved 3.5 billion years ago on Mars when hydrothermal systems are
believed to have been active (26, 40). Our application of
18Op as a biomarker
demonstrates that 18Op
values can successfully detect enzymatic activity and microbial metabolism in terrestrial systems. These systems serve as important analogues for extraterrestrial environments that are targeted in the
search for life because of the possible presence of liquid water. The
18Op biomarker should
provide strong evidence for the presence of life.
| |
Acknowledgements |
We thank G. A. Garcia for helpful suggestions in the design of
enzyme experiments and J. R. O'Neil and J. P. Greenwood for fruitful discussions and helpful comments. Thanks also go to N. F. Moreira and D. LeBlanc for field sampling support and analysis. This
work was supported in part by: National Science Foundation Postdoctoral
Fellowship (awarded to R.E.B., 1998); Bateman Postdoctoral Research
Award (R.E.B., Yale University, 1998); and National Science Foundation
Grant OCE-00-82416.
| |
Footnotes |
To whom reprint requests should be addressed. E-mail:
blake{at}geology.yale.edu
This paper was submitted
directly (Track II) to the
PNAS office.
¶
Dreibus, G., Bruckner, J. & Wanke, H. Lunar Planet.
Sci. XXXI, 31, 1127 (abstr.).
Moreira, N. F., Martini, A. M. & Blake, R. E., Northeast Section Meeting of the Geological Society
of America, March 2000, New Brunswick, NJ (abstr.).
| |
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Abstract
Introduction
18OP...
