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PREBIOTIC PHOSPHORUS CHEMISTRY RECONSIDERED*

ALAN W. SCHWARTZEvolutionary Biology Research Group, Faculty of Science, University of Nijmegen, Toernooivelcl,

6525 ED Nijmegen, The Netherlands

(Received 7 November, 1996)

Abstract. The available evidence indicates that the origin of life on Earth certainly occurred earlier than 3.5 billion years ago and perhaps substantially earlier. The time available for the chemical evolution which must have preceded this event is more difficult to estimate. Both endogenic and exogenic contributions to chemical evolution have been considered; i.e., from chemical reactions in a primitive atmosphere, or by introduction in the interiors of comets and/or meteorites. It is argued, however, that the phosphorus chemistry of Earth’s earliest hydrosphere, whether primarily exogenic or endogenic in origin, was most likely dominated by compounds less oxidized than phosphoric acid and its esters. A scenario is presented for the early production of a suite of reactive phosphonic acid derivatives, the properties of which may have foreshadowed the later appearance of biophosphates.

1. The Earth’s Atmosphere and the Origin of Life

It is clear that life was present on Earth at least 3.5 billion yr ago (3.5 Ga; Schopf and Packer, 1987) and isotopie arguments would date the origin of life even earlier (Shidlowski et al., 1983; Mojzsis et al., 1996). Less easy to assess is the period of time which would have been available for chemical evolution. The delimiting factors which need to be taken into consideration are: the timing of core forma­tion and the completion of outgassing, the effect of impacts on the stability and composition of an early outgassed atmosphere, and the timing of the appearance of the first stable accumulations of liquid water. Although arguments have been presented that permanent bodies of water may not have been stable prior to 3.8 Ga (Sleep et al., 1989), geological evidence suggests an earlier date (Mojzsis et a l ,1996). The critical stages in the evolution of organic phosphorus-containing com­pounds, however, may have occurred very early indeed. As I hope to show below, there are reasons to think that in both an early outgassed atmosphere, as well as in an atmosphere produced largely by volatiles introduced by impactors, phosphorus would have been present in a gaseous form such as phosphine (PH3) or, initially, even as free phosphorus (P2 or P4).

2. Apatite and Other Phosphate Minerals

Although it has long been recognized by geologists that the only significant form of phosphorus in the Earth’s crust is apatite in its various mineralogical mani­festations, solubility arguments suggest that little if any organic chemistry in the

* Paper dedicated to Leslie Orgel on the occasion of his seventieth birthday.

Origins o f Life and Evolution of the Biosphere 27: 505-512, 1997.(c) 1997 Kluwer Academic Publishers. Printed in the Netherlands.

506 A. W. SCHWARTZ

O

HP----- OHH

Hypophosphorous

Acid

O

H OH

OH

Phosphorous

Acid

O

HO-----P----- OH

OH

Orthophosphoric

Acid

Figure I . The Stuctures of the two lower oxyacids of phosphorus - hypophosphorous and phosphorous acids - and of phosphoric acid. Inorganic salts of the acids are referred to as hypophosphites, phosphites and phosphates, respectively.

primitive oceans could have resulted from this source, at least in the absence of some additional mechanism for concentrating and activating phosphate. An ear­ly contribution of Orgel to this field was the demonstration that hydroxyapatite could directly serve as a source of phosphate for the solid state phosphorylation of nucleosides in the presence of ammonium chloride and urea (Lohrmann and Orgel, 1971). A not dissimilar synthesis of nucleotides utilizing apatite in the pres­ence of ammonium oxalate and any of several organic activating agents was also published by the present author (Schwartz, 1972a). In later work, the proposal that phosphate minerals other than apatite would precipitate under prebiotic conditions was explored by Handschuh and Orgel (1973) and phosphorylation of nucleosides with the mineral struvite was demonstrated. A more complete discussion of these and related topics is to be found in the paper by Kolb et al., elsewhere in this issue (Kolb et al., 1997). In attempting to evaluate the probability of prebiotic scenarios, it has often proved useful to turn to the only readily accessible source of ‘primitive’ material available to us; the carbonaceous chondrites. It is this approach which has recently led me to explore a rather different scenario.

3. Lower Oxyacids of Phosphorus

The only phosphorus-containing organic compounds which have been found in carbonaceous chondrites are the alkyl phosphonic acids reported by Cooper et al., in the Murchison meteorite (1992). These molecules can be viewed as deriving from a source of phosphorus more reduced than orthophosphate. These authors pointed out that the C-P bond in the phosphonic acids may be derived from CP, which has been observed in the carbon rich circumstellar envelope IRC+10216 by Guélin et al. (1990). Gulick (1955) was probably the first to suggest an exogenic source of phosphorus. He supposed that hydrolysis of meteoritic schreibersite (Fe2NiP) might produce hypophosphorous acid. Because hypophosphite is easily oxidized, phosphite and ultimately phosphate are also logical products (Figure 1). As Gulick pointed out, both hypophosphite and phosphite are considerably more soluble as calcium salts than is phosphate. Hydrolysis of schreibersite has also been considered as a source of both phosphine and phosphorous acid (Schwartz, 1972b;

PREBIOTIC PHOSPHORUS CHEMISTRY RECONSIDERED 507

Holland, 1984). Of perhaps even greater significance, however, is the possibility that the process of core formation in the early Earth may have resulted in massive outgassing of elemental phosphorus. This argument has been presented before (Schwartz, 1972b), but recent results make it a worthwhile exercise to summarize the basic points. It was suggested that the formation of schreibersite inclusions within iron meteorites was most likely the consequence of the reduction of apatite by carbonaceous material during chemical differentiation of the meteorite parent body. By analogy, a similar process would have occurred on Earth. An industrial process for the manufacture of phosphorus is, as a matter of fact, based on this reaction, which can be summarized as

Ca3(P04)2 + 3Si02 + 5C->3CaSi03 + 5CO + P2 ( 1 )

(Jacob and Reynolds, 1928).

Oxidation of the phosphorus so produced would ultimately yield phosphate. How­ever, studies of the oxidation of phosphorus by steam (in the absence of 0 2) have shown that significant amounts of phosphorus tetroxide and phosphine are pro­duced (Brunauer and Shultz, 1941). Since the hydrolysis product of phosphorus tetroxide is phosphorous acid (Van Wazer, 1958), it is possible that the first liq­uid water to condense on Earth contained a significant proportion of phosphorous acid, and that phosphites (the inorganic salts of phosphorous acid) would therefore have been present in the early hydrosphere.* Source and solubility considerations, therefore, suggest a more important role for the lower oxyacids of phosphorus in early chemical evolution than for phosphate. Additionally, the presence of the P-H bond in phosphite creates new chemical possibilities.

4. Phosphonic Acids and Prebiotic Chemistry

The irradiation of phosphite solutions with ultraviolet light results in the generation of phosphite radicals, which can combine with other radicals or add to an unsat­urated bond. We have recently demonstrated that the products shown in Figure 2 can be generated in this manner starting with phosphite (De Graaf et a i , 1995 and1997). AU the compounds shown are easily soluble in water, even in the presence of excess calcium. One of the most interesting products is vinyl phosphonic acid (VPA), which is produced by addition of a phosphite radical to acetylene (Figure 3;

* A reviewer points out that outgassing as a result of core formation could have had catastrophic consequences for the survival of reduced phosphorus due to the greenhouse properties of a dense CO2+H2O atmosphere. A small scale version of the above scenario, however, perhaps occurring after solar wind- induced loss of the initial outgassed atmosphere, can also be imagined to have occurred during ablation of carbonaceous chondrite-like impactors. Once a more hospitable atmosphere had been established, phosphorous acid as well as phosphonic acids would rapidly have rained out of the atmosphere.

508 A. W. SCHWARTZ

HHC

HO

OH

MPA

OH O

1-HEPA

OH O

HCH

O

OH

HMPA 2-HEPA

HHO

H

HC-H

O

*P— O'

OH

EPA

O

o—c HCH

O

P— O

OH

PAA

HGH

HC

O

P— O’ VPA

OH

O

HCHCH

OH

PAL

Figure 2, Phosphonic acids in meteorites and from model prebiotic syntheses. MPA, methyl phos­phonic acid; HMPA, hydroxy methyl phosphonic acid; EPA, ethyl phosphonic acid; VPA, vinyl phos­phonic acid; 1-HEPA, 1-hydroxyethyl phosphonic acid; 2-HEPA, 2-hydroxyethyl phosphonic acid; PAA, phosphonoacetic acid; PAL, phosphonoacetaldehyde. MPA and EPA are Murchison meteorite components (Cooper et al., 1992). MPA has been synthesized by ultraviolet irradiation of phosphite in the presence of acetone and HMPA in the presence of formaldehyde or methanol (De Graaf et a i, 1995). VPA has been synthesized by ultraviolet irradiation of phosphite in the presence of acetylene, and the remaining compounds are all produced by photolysis of VPA (De Graaf et al., 1997).

O

HP— O

OH

Ouv

H +H C = CH

O

OH

HC:H

HC

O

P— 0

OH

Figure 3. The formation of vinyl phosphonic acid via the addition of a phosphite radical to acetylene.

De Graaf et al. 1997). VPA can, in turn, undergo subsequent photolysis to pro­duce a variety of oxygenated products. Of these, phosphonoacetaldehyde (PAL) is particularly interesting since it is an analogue of glycolaldehyde phosphate. The latter compound was shown by Müller et al. (1990) to undergo a two step, base-catalyzed condensation in the presence of formaldehyde to produce ribose- 2,4-diphosphate. Although PAL is only generated in modest yield by photolysis of VPA (4 to 10%, depending on pH), it avidly undergoes base-catalyzed conden­sation. By analogy with the pathway discovered by Müller et a i , it is possible to imagine the sequence of reactions shown in Figure 4, leading to the formation

PREBIOTIC PHOSPHORUS CHEMISTRY RECONSIDERED 509

CHO O CHO

HC-H

P'I

0

«

0H2CO

HC-OII

■p—oOH, H+

1HCOH 0 .

H

CHO

HOH

011 AP— o1

o .

+

CHO

HO0

P— O

HCOH O H

'OH, H+--------->_2

CHO

HO

HCOH

HO

HCOHH

OI!p -o0 _OII

ÎO

o

CHO

HC

HCOH

HO

HCOHH

?\?r oo mo

o

O

O—P—-I

_0

Figure 4. Suggested reaction pathway for the production of 2,4-dideoxyribose-2,4-diphosphonic acid from phosphonoacetaldehyde in the presence of one-half equivalent of formaldehyde.

o f 2J4-dideoxyribose-2,4-diphosphonic acid. Reaction 1, the aldol condensation of phosphonoacetaldehyde with formaldehyde has been demonstrated to occur effi­ciently and selectively (De Graaf, unpublished data). Reaction 2, the condensation o f PAL with 2-deoxyglyceraldehyde-2-phosphonic acid is currently under study. Reaction 3 shows the expected formation of the pyranose form of the compound.

Carrying this analogy a step further, let us consider the properties of a nucleotide analogue based on this compound in place of ribose-2 ,4 -diphosphate. Activation o f both phosphonic acid groups should lead to oligomerization through the for­mation of pyrophosphonic acid linkages (Figure 5). The competing reaction of intramolecular cyclization of either phosphonic acid group with the 3 ’ -hydroxyl is improbable as it would lead to the formation of a four-membered phosphonic acid ester ring. Computer modeling studies have also shown that internal condensation of the two phosphonic acid groups to form a 2’,4’-pyrophosphonic acid ring is dis-

510 A. W. SCHWARTZ

O

BASE

HO-'

BASE

BASE

Figure 5. Hypothetical oligomerization of a nucleotide analogue based on 2,4-dideoxyribose-2,4- diphosphonic acid to produce a pyrophosphonic acid-linked chain, as a result of chemical activation and condensation of the phosphonic acid groups.

favored as well. Experience in the formation of pyrophosphate-linked chains via the activation of 3’-deoxynucleoside-2\5’-diphosphates supports the suggestion that oligomerization would readily occur (Visscher and Schwartz, 1987). Notice that the repeating unit in the oligomer produced is composed of six atoms, as in Eschenmoser’s pyranosyl-RNA (p-RNA) and, of course, RNA itself (Pitsch et al., 1993).

To test the possibility that such an analogue might be capable of forming a double-helical structure similar to that displayed by p-RNA, a model was con-

PREBIOTIC PHOSPHORUS CHEMISTRY RECONSIDERED 511

v.;.; X ^v,v» X ?X'M' 'S: !• v ',v;

w . 'x o ; . ; . • ; ; .;.y0!;X '.v ■. y ;f v- ; y J \y r r v v- ¡ > ^ ;>i « • i i J % • • » » V * « • « \ * r • . « « « • • . * . « ' W • ' . .* . V, i I V i t « ' 1 • • T I • • • 1 ®| « V « ...........................

* Ì i ! Ì I i , y ' ^' ^ ƒ ¡»'y \ ̂''' ' ̂ y ^ f '*** ̂' '' '' '' '' ' ^ 'J - lv X o l-S v .. * .v>'»yi' 'v v ’• «'—«v ' V’v * \ • .* '* « «

Figure 6. Double-helical model (Maruzen Co.) showing complementary, pyrophosphonic acid linked dodecamers of nucleotide analogues based on 2,4-dideoxyribose-2,4-diphosphonic acid.

512 A. W. SCHWARTZ

structed and is shown in Figure 6 . The properties of the structure indeed appear to be generally similar to those of p-RNA. There is a pronounced inclination between the helical axis and the plane of the base pairs. Consequently, the bases are stacked ‘intermolecularly’: one base in each pair is stacked onto the complement of its neighbor in the 2 ’-direction, while the complement is stacked onto the comple­ment of its neighbor in the 4 ’-direction. The vertical distance between base pairs averages about 5.0 Â and the general form of the duplex is a left-handed, helically coiled ribbon with a pitch of roughly 55 Â. The rather large base pair raise of 5.0 Â appears to be optimal for this molecule, as reducing the distance would produce an unacceptably close approach of the hydrogen atoms on C5 of the pyranose rings with the plane of the base pairs. Formally, of course, the construction of a model merely demonstrates that the proposed structure is not impossible. However, the properties of the model do encourage further research.

Acknowledgment

This work was partially supported by U.S. National Aeronautics and Space Admin­istration grant NAGW-1660.

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Carriers of Phosphorus’, /, Mol. EvoL 44, 237.Guelin, M., Cemicharo, J., Paubert, G. and Turner, B. E.: 1990, Astron. Astophys. 230, L9.Gulick, A.: 1955, Scientist 43, 479.Handschuh, G. J. and Orgel, L. E.: 1973, Science 179, 483.Holland, H. D.: 1984, The Chemical Evolution o f the Atmosphere and Oceans, Princeton University

Press, Princeton, N.J., pp. 116-120.Lohrmann, R. and Orgel, L. E.: 1971, Science 171, 490.Jacob, K. D. and Reynolds, D. S.: 1928, Indust Eng. Chem. 20, 1204.Kolb, V., Zhang, S., Xu, Y. and Arrhenius, G.: 1997, ‘Mineral Induced Phosphorylation of Glycolate

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and Biological, Plenum Press, New York, pp. 129-140.Sleep, N. H., Zahnle, K. J., Kasting, J. F. and Morowitz, H. J.: 1989, Nature 342, 139.Van Wazer, J. R.: 1958, Phosphorus And Its Compounds, Interscience Publishers, New York. Visscher, J. and Schwartz, A. W.: 1987, J. M ol EvoL 26, 291.