Phil. Trans. R. Soc.

B (2006) 361, 1743–1749

doi:10.1098/rstb.2006.1901
Published online 7 September 2006

Phosphorus in prebiotic chemistry

Alan W. Schwartz*
Radboud University Nijmegen, Nijmegen 6500, The Netherlands
The prebiotic synthesis of phosphorus-containing compounds—such as nucleotides and poly-
nucleotides—would require both a geologically plausible source of the element and pathways for its
incorporation into chemical systems on the primitive Earth. The mineral apatite, which is the only
significant source of phosphate on Earth, has long been thought to be problematical in this respect
due to its low solubility and reactivity. However, in the last decade or so, at least two pathways have
been demonstrated which would circumvent these perceived problems. In addition, recent results
would seem to suggest an additional, extraterrestrial source of reactive phosphorus. It appears that
the ‘phosphorus problem’ is no longer the stumbling block which it was once thought to be.
Keywords: prebiotic phosphorylation; sources of phosphate; primitive Earth; reducing conditions;
volcanic lightning

1. INTRODUCTION I have tried to find a basis for the biological selection of

We have all become quite accustomed to referring to S and P for group and energy transfer reactions in (1)
the so-called biogenic elements—designated by the the fact that they form more open and usually weaker
chemical symbols CHNOPS—without too much bonds than their cogeners in the Second Period [of the
reflection as to why these elements play the role in periodic table], O and N; (2) their possession of 3d
biology that they do. However, a small group of notable orbitals, permitting the expansion of their valences
beyond four; and (3) their retention of the capacity to
scholars has addressed the question ‘why’. Lawrence
form multiple bonds, a property otherwise charac-
Henderson (1913), for example, in a book entitled
teristic of C, N, and O. The capacity to form multiple
The fitness of the environment, pointed out that certain bonds contributes principally to the thermodynamics
features of the environment were admirably suited to of energy transfer.
support life. Henderson (who is still well-worth reading
by today’s astrobiologists) pointed to (among other Also of interest in this connection, are the remarks of
phenomena) the now famous example of the anom- Todd (1959):
alous expansion of water at the freezing point. This This discussion of phosphate chemistry is by no means
property leads to the fact that the oceans do not freeze complete, but enough has been said to indicate in some
solid as a result of several cold winters, but rather freeze degree why phosphate derivatives occur so widely as
each winter from the top-down, and consequently, are reactive intermediates in biological systems. Some of
able to melt again during the summer. Other charac- the reactions I have discussed can be simulated by
teristics of water considered by Henderson included derivatives of other acids, but the tribasic character of
other thermal properties such as its high specific heat, phosphoric acid gives it the tremendous flexibility in
latent heat of melting and of evaporation, thermal action which makes it almost ideal as a multi-purpose
conductivity and solvent properties. This approach was reagent in living processes.
followed and expanded on by Blum (1951), in his book Frank Westheimer (1987) has also added to the
Time’s arrow and evolution. Subsequently, George Wald literature on this subject, and pointed to a number of
(1958), in an introduction to the 1958 edition of properties of phosphate which fit this group for its role
Henderson’s book, pointed out that H, O, N and C in both energy transfer and as a backbone feature of
constitute 99% of all examples of living tissue and nucleic acids.
offered as a reason the fact that these four elements are In light of the above arguments, we should not be
(in that order) the smallest in the periodic table which surprised by the central role which phosphorus plays in
reach stable electronic configurations by adding, biology, and presumably, must also have played in the
respectively, 1, 2, 3 and 4 electrons. In other words, origin of life. From the point of view of prebiotic
they are the simplest elements able to form bonds, and chemistry, the next logical question is what was the
particularly (also as a result of their smallness), exact sequence of events that started with inorganic
multiple bonds. In a later discussion of the same materials, and led to the formation of the first
general topic, Wald (1962) expanded the argument to P important organic phosphate compounds. Since ATP
and S: is the central phosphorus-containing metabolite in
biology and is involved in virtually all phosphorylation
reactions, we could do worse than begin with the
*[email protected] question of its synthesis and properties. A valuable
One contribution of 19 to a Discussion Meeting Issue ‘Conditions for observation in this regard was made by Jones &
the emergence of life on the early Earth’. Lipmann (1960), who suggested that the role of ATP

1743 This journal is q 2006 The Royal Society

1744 A. W. Schwartz Phosphorus in prebiotic chemistry

(a)
O
∆
n (NH4)2 HPO4 HO P O H + 2n NH3 + n–1 H2O
O
H n
(b)
O O O O
_ _ _ _ _ _ _
ROH + HO P _ O P OH RO P OH + HO P OH

O O O O
H H H H
Figure 1. (a) Balanced, idealized reaction equation for the production of condensed phosphates by the heating of ammonium
phosphate at elevated temperatures (greater than 1258C). In an actual experiment, of course, the reaction may not be complete.
(b) Reaction of an alcohol or nucleoside with pyrophosphoric acid (the simplest, but least reactive example of a condensed
phosphate) to produce a phosphate monoester with elimination of phosphoric acid.

might have been preceded in prebiological chemistry photolysis to N2 (Ferris & Nicodem 1974). For this
by inorganic polyphosphates: reason, the most reasonable scenario may be one
involving the recycling of ammonia. For example,
The inorganic polyphosphates which are found in a
ammonia is generated by hydrolysis of many potentially
great variety of organisms seem more attractive as
primary donors. Although now they give the
important prebiotic reactants such as nitriles and
impression of being metabolically fairly inert, they amides. Thus, it is not difficult to imagine it being
may represent an early means of energy distribution continually regenerated in solution, at least locally. The
which was abandoned later on. Their availability from photochemical and geochemical cycling of ammonia is
inorganic sources seems to be rather likely. a complex problem, involving a number of processes.
For a review and perspective on these questions, see
This observation provided a strong impetus for Summers (1999).
investigations into the properties of inorganic polypho- As is often the case in prebiotic scenarios, a volcanic
sphates and their utility in phosphorylation reactions. region would seem to be the sort of locale where
polyphosphates as well as phosphorylation reactions
could be driven by ammonium salts of phosphoric acid.
2. PHOSPHORYLATION REACTIONS While there is no shortage of models of prebiotic
WITH POLYPHOSPHATES OR phosphorylation in the literature, we need properly to
AMMONIUM PHOSPHATES deal first with the question of the source material on the
In synthetic organic chemistry, reactive and usually primitive Earth for all subsequent phosphorus chemi-
unsaturated ‘condensing agents’ are commonly stry. The phosphorylation methods summarized earlier
employed for phosphorylation reactions. A number of are all subject to the criticism that they do not utilize a
studies of possible ‘prebiotic’ phosphorylations have geologically plausible source of phosphate. In other
therefore utilized reactive compounds such as cyana- words, where did the phosphate come from in the first
mide and various related compounds (Steinman et al. place?
1964). Probably the most convincing models of
prebiotic phosphorylations, however, have made use
of inorganic polyphosphates or salts of phosphoric acid, 3. KNOWN SOURCES OF INORGANIC
which yield polyphosphates upon heating. A general PHOSPHATE
summary of this approach is shown in figure 1. A summary of the most important naturally occurring
Figure 1 summarizes the reactions involved in the phosphate minerals, both on the Earth and in
thermal phosphorylation of a nucleoside by heating in meteorites, is shown in table 1 (the most important
the presence of ammonium phosphate (Rabinowitz structural forms are shown; in actual fact, most
et al. 1968). The structure given as HO[PO3H]nH is occurrences involve a mixture of species).
the average composition of condensed phosphate of We are at once confronted by a problem in viewing
chain length n. At a moderate temperature such as this list. With the possible exception of meteoritic
1258C, the primary products are pyrophosphate and schreibersite (to be discussed later), all of the
tripolyphosphate. At elevated temperatures, long- compounds in table 1 are only slightly soluble in
chain polyphosphoric acid is formed. Solid-state water. While organisms can make use of the micromolar
phosphorylations such as these have been shown to concentrations of phosphate which occur in natural
be catalysed by urea (Lohrmann & Orgel 1971). Under waters, it is difficult to imagine how any useful synthetic
these conditions, the escape of gaseous ammonia as (prebiotic) chemistry could take place. Owing to the
well as water provides the driving force. Once formed, high natural abundance of calcium, evaporation of
polyphosphates are effective phosphorylating seawater does not lead to an increase in phosphate
agents, even in neutral aqueous solution (Schwartz & concentration, but to precipitation of one or another
Ponnamperuma 1968). There is some question as to form of apatite or francolite. Two possible exceptions to
the availability of ammonia on the primitive Earth, due this general behaviour should be noted. Firstly, if the
to its rapid photolytic conversion by ultraviolet early oceans were slightly less alkaline than today’s

Phil. Trans. R. Soc. B (2006)

 Phosphorus in prebiotic chemistry A. W. Schwartz 1745

Table 1. Some naturally occurring phosphorus-containing minerals.

fluorapatite Ca5(PO4)3F terrestrial igneous minerals, meteorites

hydroxyapatite Ca5(PO4)3(OH) terrestrial sedimentary minerals
francolite Ca5(PO4)2.5(CO3)0.5F terrestrial sedimentary minerals
schreibersite (Fe, Ni)3P meteorites
whitlockite Ca9(Mg, Fe)(PO4)6PO3OH meteorites
chlorapatite Ca5(PO4)3Cl meteorites

O O O

HO P OH HO P OH H P OH

OH H H

phosphoric acid phosphorous acid hypophosphorous acid

Figure 2. The three oxyacids of phosphorus. The salts are referred to as phosphates, phosphites and hypophosphites,
respectively.

oceans, perhaps due to a higher partial CO2 pressure, 4. LIGHTNING IN VOLCANIC ERUPTION CLOUDS
then the precipitation of the acid calcium salt brushite AND PHOSPHATE
(CaHPO4$2H2O) might have been possible (Gedulin & A phenomenon familiar to volcanologists is the
Arrhenius 1994). Secondly, under conditions of occurrence of lightning discharges in eruption clouds.
relatively high magnesium and ammonia concen- Gilbert & Lane (1994), for example, in a specialist
trations, an additional precipitate becomes possible report related to the topic of aviation safety, cite
(Handschuh & Orgel 1973), the mineral struvite multiple cases of lightning in volcanic clouds, which
(MgNH4PO4$6H2O). Both of these latter minerals were observed during eruptions at 11 different
can generate condensed phosphates upon heating. volcanoes, while Navarro-Gonzalez et al. (1996) list
We have to go back to Addison Gulick (1955) to an additional six documented examples and yet more
find the first explicit discussion of the problem of the can be found on the Internet. Two features of these
low solubility of phosphate minerals, as well as a events make them interesting from the point of view of
suggestion as to a possible solution. Gulick pointed prebiotic chemistry: (i) the presence of reduced gases in
out that the only significant source for phosphorus on volcanic eruptions and (ii) the presence of abundant
Earth was the slightly soluble mineral apatite. He dust in the clouds. It was pointed out by Russian
suggested that under the supposed ‘reducing con- workers in the 1970s that these conditions were
ditions’ described by Oparin (1938) as well as Urey suitable for prebiotic syntheses such as the Miller
(1952), phosphate would be reduced to a form such experiment and a number of kinds of organic
as phosphite or hypophosphite (figure 2), which are compounds, including amino acids, were identified
considerably more soluble in the presence of calcium (chiefly by paper and thin-layer chromatography) in
than phosphate. volcanic deposits (e.g. Markhinin & Podkletnov 1977).
This suggestion was considered by Miller & Urey Today, we would require more definitive molecular
(1959), who noted that all the lower oxidation states characterization of compounds of potentially biological
of phosphorus were unstable under the pressures of significance than were then applied, as well as evidence
hydrogen which these authors found to be probable that they were not introduced by contamination.
for the primitive Earth. Although they remarked that Nevertheless, conditions such as those described earlier
stronger reducing agents than hydrogen might have also raise the possibility of reduction of phosphate to
been present and that such a possibility was phosphite. In a simulation of the process, we have
deserving of further investigation, the possibility found that reduction is surprisingly effective, but
that reduction of phosphate could have occurred strongly dependent on the reducing nature of the gas-
under unusual conditions actually remained unad- mixture employed (figures 3 and 4).
dressed. Recent work has shown that such a process The interest of phosphite as a possible prebiotic
is indeed possible. This review will describe three phosphorus source is not only due to the higher solubility
scenarios by means of which phosphate could have of its calcium salt compared to apatite (approx. 1000
been made available for prebiotic chemistry. The first times higher),1 but also to its greater reactivity as a
is the possibility of phosphate reduction by a phosphorylating agent. It has been established that
combination of reducing and high-energy conditions. ammonium phosphite, for example, readily reacts with
The second is the discovery by Yamagata et al. that nucleosides to yield nucleoside-phosphites (nucleoside
P4O10 can be volatilized from magma and is, in fact, H-phosphonates) under conditions in which
being liberated from contemporary volcanoes. The ammonium phosphate is unreactive (figure 5).
third scenario is related to a recent demonstration We have shown that nucleoside H-phosphonates are
that the meteoritic phosphide mineral schreibersite is easily synthesized. Preliminary results also indicate that
surprisingly reactive. they are thermally condensed to form dimers linked by

Phil. Trans. R. Soc. B (2006)

1746 A. W. Schwartz Phosphorus in prebiotic chemistry

Figure 3. Apparatus used to study the effect of electric discharge on mineral samples. Samples of apatite, mixed with a clay
mineral to provide improved adhesion, were deposited onto the ends of an open tungsten loop, which formed a gap of a few
millimetres. Pyrex caps (not shown) were fitted over the ends of the loop to prevent direct interaction of the sample with the
metal. The chamber was evacuated and back-filled with the gas mixture to be tested. A spark was induced between the ends of
the loop by exposing the apparatus to a microwave field. (Illustration from Glindemann et al. 1999; reproduced with kind
permission of Springer Science and Business Media.)

yield of phosphite versus 'reducing content' of gas mixtures %

30 50
40
25
phosphite yield (%)

30
20
20
15 10

10
0 5 10 15 20 25
time (h)
5
Figure 5. Yield of uridine-5 0 -phosphite by reaction of uridine
with ammonium phosphite (1 : 2 molar ratio) at 608C. Solid
0 5 10 15 20
squares, four sets of reactions giving the yields in the absence
Figure 4. The conversion of apatite to phosphite by spark of urea; solid circles (upper series of data points), yields in the
discharge in a model atmosphere containing initially 60% presence of urea (uridine : ammonium phosphate : ureaZ
CO2 and 40% N2, but with increasing additions of H2 and 1 : 2 : 4). The initial time-lag observed for 5 h and less was
CO (the abscissa shows the sum of the contents of H2 probably due to the evaporation of water from the reaction.
and CO, which were present in equal concentrations). Data Under identical conditions as those shown here, ammonium
points (solid squares) are averages of three to five replicate phosphate produced no products (De Graaf & Schwartz
analyses and the vertical lines show the average deviation of 2005; reproduced with kind permission of Springer Science
the mean of each set of measurements (De Graaf & Schwartz and Business Media).
2000; reproduced with kind permission of Springer Science
and Business Media).
5. VOLATILIZATION OF P4O10 AND GENERATION
H-phosphonate diester bonds. While the monomers OF POLYPHOSPHATES IN VOLCANIC REGIONS
are resistant to oxidation, once incorporated into a Yamagata et al. (1991) reported the detection of
dimer, the linkage is easily oxidized to a phosphodie- condensed phosphates (primarily pyrophosphate and
ster. It is, therefore, conceivable that they might act as tripolyphosphate) in condensates from experiments in
intermediates in a pathway towards the formation of which apatite mixed with basalt had been subjected to
polynucleotides, as illustrated in figure 6. elevated temperature, thus indirectly confirming an
Phosphite, incidentally, also provides a possible link to earlier prediction that P4O10 would be volatilized from
the presence of phosphonic acids in carbonaceous apatite at high temperature (Griffith et al. 1977). More
chondrites. These compounds, which are the only striking was the identification of the same products in
phosphorus-containing organic compounds to be ident- condensates collected from a fumarole of the volcano
ified in meteorites, were reported by Cooper et al. (1992) Mount Usu. The concentrations reported for ortho-
in investigations of the Murchison meteorite (figure 7). phosphate, pyrophosphate and tripolyphosphate were
An interesting possibility concerning the mechanism 1.13, 0.45 and 0.37 mM, respectively. These concen-
of synthesis of these compounds in meteorites is that trations are very low and it is perhaps unlikely that they
they might derive from reactions of the PO3 radical could have contributed directly to chemical evolution.
di-anion and thus, ultimately, from a source such as More interesting is the question of the possible
phosphorous acid or phosphites. For example, recom- interaction of condensed phosphates with organic
bination of %PO3 with a methyl radical has been shown products on the surfaces (and perhaps even absorbed
to produce methyl phosphonic acid, the most abundant into the interior) of ash particles in eruption clouds. In
phosphorus-containing compound in Murchison. the course of the experiments on phosphite production
Similarly, a suite of other phosphonic acids has been mentioned earlier, we were also able to detect ortho-
synthesized via ultraviolet irradiation of phosphite in pyro- and tripolyphosphate, essentially confirming the
the presence of formaldehyde or simple alcohols results of Yamagata et al. In our experiments, up to 50%
(De Graaf et al. 1995). of the phosphate exposed to the electric discharge was

Phil. Trans. R. Soc. B (2006)

 Phosphorus in prebiotic chemistry A. W. Schwartz 1747

O O B O O B

O– O O O O

O PH O PH O P O–

O O B O O B O O B

HO OH O O O O

nucleoside phosphite (H-phosphonate) H-phosphonate diester linkage phosphodiester linkage

Figure 6. A hypothetical pathway starting with a nucleoside phosphite, leading to the formation of nucleoside-3 0 -5 0 H-
phosphonate linkages and, finally, to 3 0 -5 0 phosphodiester linkages. While oxidation of a nucleoside H-phosphonate (monomer)
is a difficult reaction, once incorporated into an H-phosphonate diester, oxidation proceeds readily with mild agents (De Graaf &
Schwartz 2005). The final step of oxidation to a phosphodiester linkage could theoretically occur on the primitive Earth by
reaction with Fe3C or HOOH. Other linkage types (such as 5 0 -5 0 , 2 0 -5 0 and so forth) are, of course, also possible.

O O O

HO P OH HO P OH HO P OH

CH3 C2H5 C3H7

methyl phosphonic acid ethyl phosphonic acid propyl phosphonic acid

Figure 7. Phosphonic acids identified in the Murchison meteorite. Note that they are all derivable from phosphorous acid in
figure 2 by replacing the hydrogen atom attached to phosphorus with a methyl-, ethyl- or propyl-group.

recovered in water extracts at the conclusion of the run, Table 2. Products obtained by reaction of Fe3P with water.
with roughly 10 and 2% of this total being in the form The reactions shown here were run in deionized water under
of pyro- and tripolyphosphate, respectively. argon as well as in the presence of air. Fe3P (1 g) was stirred in
25 ml H2O for 1 day at 208C (selected data from Pasek &
Lauretta 2005).

6. SCHREIBERSITE AS A POSSIBLE PREBIOTIC mM concentration

SOURCE OF CONDENSED PHOSPHATES
Recently, an additional possibility and potential source product in argon in air
of reactive phosphorus compounds has been suggested
by Pasek & Lauretta (2005). As was noted in table 1, orthophosphate ðPO3K
4 Þ 130 1100
the phosphide mineral schreibersite is a well-known orthophosphite ðHPO2K3 Þ 100 700
inclusion in iron meteorites and enstatite chondrites, hypophosphate ðP2 O4K
6 Þ 18 280
generally in the form of discrete nodules or grains. pyrophosphate ðP2 O4K
7 Þ 23 150
These authors estimate that as much as 5% of total
crustal P was at one time extraterrestrial schreibersite,
added to the Earth by impacts during or at the end of A mechanism which would explain the higher yields
the late heavy bombardment. However, the most observed in the presence of oxygen has not yet been
interesting result of this new work is an investigation elucidated. Remarkably, however, pyrophosphate at a
of the aqueous chemistry of the compound Fe3P, which concentration of 23 mM was observed even under
was used to approximate schreibersite. Since the argon. The authors speculate that hypophosphate is
valance level of phosphorus in the mineral is 0 and it the precursor of the pyrophosphate detected (figure 8).
is known to consist of a solid solution of the element in Although this concentration seems low, it is at least
the meteoritic Fe–Ni phase, it might have been an order of magnitude higher than the solubility of
expected to be rather unreactive and not produce apatite as well as representing an activated form of
much novel chemistry upon introduction into water. phosphate which itself can, under certain conditions,
Quite surprisingly, however, reaction of synthetic Fe3P produce phosphorylated products (Neuman et al.
with pure water as well as with saline or other salt 1970). More data on this interesting reaction are clearly
solutions was found to rapidly produce condensed desirable, particularly if the results can be repeated with
phosphate as well as hypophosphate, a compound authentic schreibersite. A poster presented at this
containing a P–P linkage. The chemistry of the reaction conference has, in fact, reported the substantiation of
appears to be quite complex, but some of the products these results with meteoritic schreibersite (Terrence
observed in a single experiment are listed in table 2. P. Kee 2006, personal communication).

Phil. Trans. R. Soc. B (2006)

1748 A. W. Schwartz Phosphorus in prebiotic chemistry

O O O O Griffith, E. J., Ponnamperuma, C. & Gabel, N. 1977

? Phosphorus, a key to life on the primitive Earth. Orig.
–O _ P _ P _ O– –O _ P _ O _ P _ P– Life 8, 71–85. (doi:10.1007/BF00927976)
Gulick, A. 1955 Phosphorus as a factor in the origin of life.
O O Am. Sci. 43, 479–489.
O O
H H H H Handschuh, G. J. & Orgel, L. E. 1973 Struvite and prebiotic
phosphorylation. Science 179, 483–484.
Figure 8. Possible formation of pyrophosphate from Henderson, L. J. 1913 The fitness of the environment: an inquiry
hypophosphate suggested by Pasek & Lauretta (2005). into the biological significance of the properties of matter.
Since hypophosphate is known to be a relatively stable Boston, MA: Macmillan.
compound under most conditions and has been synthesized Jones, M. E. & Lipmann, F. 1960 Chemical and enzymatic
by UV irradiation of phosphite, this is a rather unexpected synthesis of carbamyl phosphate. Proc. Natl Acad. Sci.
consequence of the reaction of Fe3P with water (Schwartz & USA 46, 1194–1205. (doi:10.1073/pnas.46.9.1194)
van der Veen 1973). Lohrmann, L. & Orgel, L. E. 1971 Urea-inorganic phosphate
mixtures as prebiotic phosphorylating agents. Science 171,
7. CONCLUSION 490–494.
A variety of pathways now are available as possible Markhinin, E. K. & Podkletnov, N. E. 1977 The phenom-
solutions for what this author used to refer to as the enon of formation of prebiological compounds in volcanic
‘phosphate problem’. The ‘problem’ seems to have processes. Orig. Life 8, 225–235. (doi:10.1007/BF009
evolved gradually into the less perplexing one of having 30684)
to decide which of several possible mechanisms are Miller & Urey 1959 Organic compound synthesis on the
most likely to have operated on the primitive Earth. primitive Earth. Science 130, 245–251.
Navarro-Gonzalez, R., Basiuk, V. A. & Rosenbaum, M. 1996
Lightning associated to Archean volcanic ash–gas clouds.
Chemical evolution: physics of the origin and evolution of
ENDNOTE life. Proc. 4th Trieste conference on chemical evolution, Trieste,
1
There appear to be no literature citations for the solubility of Italy, 4–8 September 1995. pp. 123–142.
CaHPO3. We have estimated this value in laboratory experiments as Neuman, M. W., Neuman, W. F. & Lane, K. 1970 On the
being greater than 0.001 M (Glindemann et al. 1999). possible role of crystals in the origins of life IV. The
phosphorylation of nucleosides. Curr. Modern Biol. 3,
277–283.
Oparin, A. I. 1938 The origin of life. New York, NY:
Macmillan. [Transl. by S. Morgulis.]
REFERENCES Pasek, M. A. & Lauretta, D. S. 2005 Aqueous corrosion of
Blum, H. F. 1951 Time’s arrow and evolution. Princeton, NJ: phosphide minerals from iron meteorites: A highly
Princeton University Press. reactive source of prebiotic phosphorus on the surface
Cooper, G. W., Onwo, W. M. & Cronin, J. R. 1992 Alkyl of the early Earth. Astrobiolgy 5, 515–535. (doi:10.1089/
phosphonic acids and sulfonic acids in the Murchison ast.2005.5.515)
meteorite. Geochim. Cosmochim. Acta 56, 4109–4115. Rabinowitz, J., Chang, S. & Ponnamperuma, C. 1968
(doi:10.1016/0016-7037(92)90023-C) Phosphorylation by way of inorganic phosphate as a
De Graaf, R. M. & Schwartz, A. W. 2000 Reduction potential prebiotic process. Nature 218, 442–443. (doi:10.
and activation of phosphate on the primitive Earth. 1038/218442a0)
Orig. Life Evol. Biosph. 30, 405–410. (doi:10.1023/ Schwartz, A. W. & Ponnamperuma, C. 1968 Phosphorylation
A:1006700512902) of adenosine with linear polyphosphate salts in aqueous
De Graaf, R. M. & Schwartz, A. W. 2005 Thermal synthesis solution. Nature 218, 443. (doi:10.1038/218443a0)
of nucleoside H-phosphonates under mild conditions. Schwartz, A. W. & van der Veen, M. 1973 Synthesis of
Orig. Life Evol. Biosph. 35, 1–10. (doi:10.1007/s11084- hypophosphate by ultraviolet irradiation of phosphite
005-0093-9) solutions. Inorg. Nucl. Chem. Lett. 9, 39–41. (doi:10.
De Graaf, R. M., Visscher, J. & Schwartz, A. W. 1995 A 1016/0020-1650(73)80083-2)
plausibly prebiotic synthesis of phosphonic aicds. Nature Steinman, G., Lemmon, R. M. & Calvin, M. 1964
378, 474–477. (doi:10.1038/378474a0) Cyanamide: a possible key compound in chemical
Ferris, J. P. & Nicodem, D. E. 1974 Ammonia: did it have a evolution. Proc. Natl Acad. Sci. USA 52, 27–30. (doi:10.
role in chemical evolution? In The origin of life and 1073/pnas.52.1.27)
evolutionary biochemistry (ed. K. Dose, S. W. Fox, G. A. Summers, D. P. 1999 Sources and sinks for ammonia and
Deborin & T. E. Pavlovskaya), pp. 107–117. New York, nitrite on the early Earth and the reaction of nitrite with
NY: Plenum Press. ammonia. Orig. Life Evol. Biosph. 29, 33–46. (doi:10.
Gedulin, B. & Arrhenius, G. 1994 Sources and geochemical 1023/A:1006517823004)
evolution of RNA precursor molecules—the role of Todd, A. 1959 Some aspects of phosphate chemistry. Proc.
phosphate. In Early life on earth (ed. S. Bengston) Nobel Natl Acad. Sci. USA 45, 1389–1397. (doi:10.1073/pnas.
symposium, vol. 84, pp. 91–110. New York, NY: 45.9.1389)
Columbia University Press. Urey, H. C. 1952 The planets, p. 245. New Haven, CT: Yale
Gilbert, J. S. & Lane, S. J. 1994 Electrical phenomena in University Press.
volcanic plumes. In Volcanic ash and aviation safety (ed. Wald, G. 1958 Introduction to Henderson. Boston, MA: Beacon
T. J. Casadevall) US geological survey bulletin, vol. 2047, Press op. cit.
pp. 31–38. Washington, DC: US Government Printing Wald, G. 1962 Life in the second and third periods; or why
Office. phosphorus and sulfur for high-energy bonds? In Horizons
Glindemann, D., De Graaf, R. M. & Schwartz, A. W. 1999 in biochemistry (ed. M. Kasha & B. Pullman), pp. 127–142.
Chemical reduction of phosphate on the primitive Earth. New York, NY: Academic Press.
Orig. Life Evol. Biosph. 29, 555–561. (doi:10.1023/ Westheimer, F. H. 1987 Why nature chose phosphates.
A:1006622900660) Science 235, 1173–1178.

Phil. Trans. R. Soc. B (2006)

 Phosphorus in prebiotic chemistry A. W. Schwartz 1749

Yamagata, Y., Watanabe, H., Saitoh, M. & Namba, T. 1991 R. J. P. Williams (Inorganic Chemistry Laboratory,
Volcanic production of polyphosphates and its relevance to University of Oxford, UK ). I think it is not necessary
prebiotic chemistry. Nature 352, 516–519. (doi:10.1038/ to postulate reduced phosphorus compounds. The
352516a0) initial requirement of cells is to get energy in a useable
form. The probability is that the first step is to make a
vesicle with a gradient of protons associated with the
Discussion membrane. This gradient will drive element uptake or
J. F. Kasting (Department of Geosciences, Penn State rejection, explaining the observed gradients of ions and
University, PA, USA). I would just note that H2/CO rich molecules essential before chemistry could occur
atmospheres, which favour phosphite over phosphate, (uphill in energy) in the prebiotic cell. We know that
are considered to be plausible prebiotic atmospheres. the proton gradient can drive the catalysed formation of
H2 may have been high (about 0.1 bar) as a conse- pyrophosphate. Given pyrophosphate (ATP) all the
quence of slow escape of hydrogen to space (Tian et al. rest of some redox chemistry—condensation—can be
2005). CO could have been abundant (O0.1 bar) in the driven.
aftermath of large impacts (Kasting, Orig. of life, 1990). A. W. Schwartz. You may well be right and experiments
Thus, getting phosphate may have been relatively easy may eventually substantiate this very reasonable
to do on the prebiotic Earth. conjecture. But this is theory rather than fact and
D. W. Deamer (Department of Chemistry and Biochem- represents a considerable extrapolation from biochem-
istry, University of California, Santa Cruz, USA). istry (i.e. requiring an enzyme) to possible prebiotic
Question: Can you please comment on the roles of chemistry. Until we have a model system, which
pH and CO2 in releasing phosphate from apatite in actually demonstrates that this can be achieved with
soluble form? plausible (simple) ingredients, it seems prudent to
A. W. Schwartz. A pH lower than in the present ocean consider other possibilities.
(about 8) would tend to increase the solubility of
apatite. Calculations have shown that at a pH between
5 and 6 (in the range which could be produced by a Additional references
high CO2 concentration), there would be about an Schwartz, A. W. 1971 Phosphate: solubilization and acti-
vation on the primitive Earth. In Chemical evolution and
order of magnitude more phosphate in solution.
the origin of life (ed. R. Buvet & C. Ponnamperuma),
Although this is still a very low phosphate concen- pp. 100–108. Amsterdam, The Netherlands: North-
tration for solution chemistry, the presence of simple Holland.
organic acids, which chelate calcium, combined with Tian, F., Toon, O. B., Pavlov, A. A. & De Sterck, H. 2005
evaporation, could strongly enhance the effect A hydrogen-rich early Earth atmosphere. Science 308,
(Schwartz 1971). 1014–1017. (doi:10.1126/science.1106983)

Phil. Trans. R. Soc. B (2006)