/. theor. Biol. (1979)81,
Hydrated
19-27
Electrons and Prebiotic Evolution J. E.
Biochemical
SCOTT
Morphology, Department University of Manchester, (Received 20 February
of Medical Biochemistry. Manchester 1979)
It is proposed that reactions of the hydrated electron e, in the “primordial soup” were an evolutionary pressure which selected biopolyelectrolytes. coacervates, “organelles” and lipid-membrane-bound structures of a pattern found in the biosphere today. The two physical restrictions of e, reactivity which determined its evolutionary specificity are (a) its exclusion from polyanion domains in Donnan fashion, and (b) its inability to solvate in alkanes. Thus, (1) polyanions (as opposed to polycations) and (2) lipid-membrane-bound (as opposed to free.) structures are protected from ea.& reactivity and degradation. The polyanionic nature of the current biosphere, and the prevalence of anionic polyanion-polycation complexes (such as ribosomes and chromatin), are attributed to (1). (2) co-operated in protecting the products of (1) as salinity in the “primordial soup” increased and (a) was no longer important. The evolution of DNA, and the existence of electron transport mechanisms are seen as logical extensions of the properties of e, Experimental evidence is already available to support all the postulated processes.
1. Introduction Theories of prebiotic biochemical evolution are necessarily teleological, with the added disadvantage that although the ends may be definable, the beginnings and intermediate stages are not, so that the means are unusually speculative. If it could be shown that given reasonable physical and chemical assumptions, an inevitable sequence of events took place leading to the defined end, this would be widely accepted as proof of the rightness of the assumptions, so small is the likelihood of the contemporary biosphere arising entirely by chance. Miller, Fox, Calvin (1969) and others took the Urey-type planet, with an atmosphere of methane, ammonia, hydrogen and water, as the point of departure, and showed that ambient physical and chemical forces would produce a “primordial soup” containing an enormous variety of monomers 19 0022-5193/79/210019+
10 %02.00/O
0 1979 Academic
Press Inc. (London)
Ltd.
20
J. E. SCOTT
and polymers similar to or identical with present-day biochemicals. How then could this random assortment of building units evolve towards highly ordered “living” systems? This note will show that there was a potent evolutionary pressure which could have led to the selection of a class of polyelectrolytes, and that this selection was an important stage on the route towards the present biosphere. Experimental evidence is available at crucial points. First, it is necessary to identify that aspect of the biosphere which is the goal of our postulated evolutionary process. 2. The Polyanionic
Nature of the Biosphere
A “balance sheet” of contemporary structural biopolyelectrolytes shows a remarkable preponderance of polyanions over polycations (Scott, 1975). Pectins, gums, slimes, alginates, acidic glycosaminoglycans and glycoproteins, nucleic acids, etc., vastly outweigh polycations, of which there are few examples (histones, protamines). The pericellular environment (connective tissue, etc.) is predominantly polyanionic, while polycations are characteristically intracellular, where their properties are not lost in the swamping excess of oppositely charged polymers. This imbalance is not surprising in an oxygen-rich atmosphere, in which polymers would tend to be oxidized, to the point of containing acidic groups as stable end products (Scott, 1975). Although this may be a good reason for the continuance of the current situation, it is difficult to see it as a prime evolutionary,cause, since free oxygen is not a feasible component of an atmosphere containing methane, hydrogen and ammonia. One would have to invoke a mysterious mechanism, arbitrarily timed, to bring about the necessary transition from a primitive to an oxygen-rich atmosphere. A better alternative, and one susceptible of experimental proof, is to look for a factor which was operative before the development of an oxygen-rich atmosphere, which would ensure that the “primordial soup” became enriched in polyanions compared with polycations. The hydrated electron (e,) first described in 1960 appears to be such an agent. It is produced by the action of ionizing radiation on water, or when an electron is released, e.g. by a P-emitting radio-active source, in water (Hart & Anbar, 1970) and is one of the most reactive species known, with a half-life of less than 1 ms. With most organic compounds, it reacts more rapidly, by several orders of magnitude. In the course of reaction with water, etc., it gives rise to other exceptionally reactive species, including H. free radicals (Hart & Anbar, 1970). Although very short-lived, its rapid rate of diffusion (about the same as
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
21
(b)
FIG. 1. Diagrammatic distributions of hydrated electrons (e-) in the electrostatic fields of (a) polyanions and (b) polycations. In (a) the polymer is shielded from the degradative attack of e, and its bye-products, by the Donnan exclusion of e,;, whereas in (b) the polymer backbone is vulnerable, because of Donnan enrichment of the polycation domain in e.; (see Scott, Davies & Ebert (1975)).
the OH- ion), ensures that it is distributed in the electrostatic fields of polyelectrolytes in the same way as other anions, i.e. it is subject to Donnan effects (Scott, Davies & Ebert, 1975). Consequently e, is excluded to a considerable degree from the domain of polyanions (Fig. l), so that the polymer is protected against the chemical reactivity of eti; and its secondary products (H .etc.). The converse is true of polycations, which concentrate e, into their domains (Fig. 1) and are thus especially vulnerable to attack by e, and its products (Scott, Davies & Ebert, 1975). es; cleaves certain bonds (e.g. the peptide bond), and H-is a highly effective degradative species. Other things being equal, polycations would therefore be chemically modified and degraded by e, at much greater rates than polyanions.
22
J. E. SCOTT
FIG. 2. Organic cations and polycations (R+) caught in the domain of a polyanion are protected from attack by e.; which is excluded from the polyanion domain in a Donnan fashion.
Some chemical structures, e.g. alcohols and ethers, are less reactive towards e.& (Hart & Anbar, 1970) and hence polysaccharides are among the more resistant polymers. Polyanionic carbohydrates would therefore be particularly resistant, compared with other biopolyelectrolytes (Scott, 1975). The negative field of the polyanion protects the polymer itself-and it also protects other species caught up within the polyanion domain (Fig. 2). Conclusive evidence is available on this point (Scott, 1975), although the relevant experiments (Balazs er al., 1968) were performed for other reasons. Organic cations (e.g. methylene blue) and polycations (polylysine) react more slowly, by an order of magnitude (Table 2) when present in solution containing an excess of polyanion (heparin) (Balazs et al., 1968a,b). This result is crucial to the theme of coacervate and organelle evolution. The pattern of this experiment (Fig. 2) is precisely that of the nucleic acids, chromatin and ribosomes.In this system, purines, pyrimidines, polycations, polypeptides, and other compounds especially reactive towards e, are protected by a negative field deriving from an enveloping polyanion. Double helical DNA presents an especially clear example. The reactive, vulnerable bases are surrounded by a cage of polyanion, which is itself of the less reactive carbohydrate type. Shragge, Michaels & Hunt (1971) showed that adenine and cytosine are lo-100 times more reactive to e& than corresponding polynucleotides, and particularly double-helical poly (A + U). The formation of nucleic acid complexes of polycations protects the
from
Scott,
Davies
& Ebert
(1975).
2.42 2.68 xx 10’ 10’
0.05 01
phthalate solution
3.7 x 10’ 1.08 x IO8 1.49 x 108
5 mM Polyvinyl in NaCIO,
Cont. of electrolyte (M) 0 OQO5 0.01
Taken
TABLE
1
0.5 mM
1.2 1.14 xx IO8 IO8
24 x tog 3.5 x lo8 2.46 x lo8
Poly-L-lysine hydrobromide in KBr solution
2 mM
Second-order rate constants (m-’ s-l) of ea; u+th polymers
3.1 x IO’
3.9 x IO7 42 x 10’
Polyvinyl-pyrrolidone in NaCIO, solution
5
s
5 ;j m
2 E
fi
z m
2
Data
from
Balazs
sulphate El-’
Ed al. (1968a,b).
47.0
32.0
Protamine 8.5~10-~
orange
0.0
26.0
43.0
M
blue
M
Alone @05
32.0
23.0
M
7.0
3.6
3.5
3.1
0.0 M
Heparin
11.6
17.5
0.05
lo--’ M
E 1-l 0.1 23.0
M
DNA
28.0
2.3
0.0
M
0.7 x 1O-4
E 1-l
TABLE 2 rate constants (1O-4 K, s-l) for the reaction of eO;with organic cations and polycations, alone or in the presence of heparin or DNA
Polylysine hydrobromide lo-“ E I-’
M
Acridine 1o-5
cont.
Methylene 1om5
NaCl
First-order
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
25
polycation from e, (Table 2, Fig. 2). In this way, primitive “chromatin” or “ribosomes” would have been evolutionarily favoured. Salinity is a factor which would have affected the selectivity of ea; as an evolutionary agent. Donnan effects are almost negligible in O-1 M NaCl, and the protective action of the polyanionic field against ea; is minimal (Scott, Davies & Ebert, 1975) (Table 1). The influence of e=; on the evolution of coacervates would have changed completely as the concentration of electrolyte in the “soup” reached isotonic levels. In more dilute electrolyte solutions, ea; and the ambient electrolyte could have collaborated in selecting polyanion-polycation complexes of high stability. Polycation-polyanion complexes are dissociated by salts, at concentrations dependent on the affinity between the interactants (Scott, 1973). Complexes formed through weak interactions can survive only dilute salt solution. At slightly higher salt concentrations the complex dissociates and the free organic cation is subject to the full attack of e&. Appropriate evidence to show this is available (Table 2). Those polyanionic complexes formed via strong interactions would survive the increasing concentrations of dissociative electrolyte and hence also degradative e.;. Specificity in the formation of polycation-polyanion complexes in the surviving “organelles” would be ensured.
3. Oxygen The conditions in which the “primordial soup” developed, viz. slight alkalinity, and an atmosphere transparent to ionizing radiation from space, ensure a high level of e, activity (Hart & Anbar, 1970). Oxygen in the atmosphere would severely restrict it by (a) reducing the level of ionizing radiation falling on the “soup”, because of the formation of the ozone layer, (b) scavenging ea; after its formation, and (c) reducing the pH of the “soup”, following the contingent disappearance of ammonia and the appearance of CO,, etc. in the atmosphere. It is a corollary of the hypothesis that the evolutionary pressure of ea&,practically ceased with the appearance of an oxygen-containing atmosphere. As pointed out above, increasing salinity would have allowed increasingly random destructive effects of e&,, because of the suppression of Donnan effects. The appearance of oxygen in the atmosphere would have effectively stabilized the status quo in the “soup” in terms of polyanion-polycation complexes. This is rather arbitrary, and does not take account of another property of e,, which could further the evolutionary process.
26
J. E. SCOTT
4. Lipid Membranes - in common with most inorganic anions, does not partition from water inzqorganic phases. It does not solvate in, e.g. alkanes (Baxendale, 1977). Thus a lipid layer acts as a barrier to e& movement. It is proposed that soaps, phospholipids and lipids formed enclosed volumes of small dimensions compared with that of the medium, and that the evolved coacervates found shelter from ambient e, within these lipid ramparts. Much evidence is available to show that this is a general phenomenon. Pyrene reacts with less than 2% of its homogenous solution rate when it is present in negatively charged lauryl sulphate micelles (Wallace & Thomas, 1973). In the neutral lecithin micelle it has less than 10yO of its homogenous solution reactivity (Schnecke, Gratzel & Henglein, 1977). Nitroanthracene and benzene show the same pattern of behaviour, serving as models for other reactive structures incorporated into lipid micelles. It is postulated that such “membrane enclosed organelles” evolved to stable organizations, utilizing interactions of the encapsulated coacervates with the inside of the membrane, e&, being the predator responsible for the scavenging of less stable organizations, or “cells”. Further protection for “cellular” structural and informational macromolecules would be derived from the presence of low molecular weight compounds with high reactivity towards e,. By capturing e& such materials would short-circuit the damaging sequence of ea< reactions. In a more advanced form, this mechanism provides a transport sysfemfor e& from the vicinity of the vulnerable macromolecules to the exterior of the “cell” or organelle, showing obvious analogies with contemporary electron transport processes in the mitochondrion, etc. This process, in a model form, has already been shown in the experiments with pyrene solutilized in lecithin micelles (Schnecke, Gratzel & Henglein, 1977). The product of pyrene and e,, a pyrene anion, detached itself rapidly from the micelle in which it was formed into the aqueous medium, where it underwent further reactions. If the pyrene anion (or analogous anionic species) reverted to pyrene in the course of these reactions, it would rapidly be re-incorporated into the micelle, thus completing the electron transfer cycle. In summary, there is compelling evidence that in an environment with a high activity of e,, as the “primordial soup” must have been, a process of selective degradation would have discriminated in favour of polyanions as opposed to polycations; of anionic complexes of polyanions with polycations, as opposed to cationic complexes of the same kind ; and of lipidmembrane-bound coacervates as opposed to free coacervates. The gradual
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
17
increase of salinity with time would have further restricted the range of coacervates which could have survived the attack of e& as well as encouraging aggregation of amphipathic molecules to form membranes and micelles. The simple operation of a cyclic scavenging mechanism for e& within these micelles would have improved the chances of survival of membrane-bound coacervates which possessed it. The evolution of a polyanion-rich biosphere would thus be only the first of several important stages in which e, was involved. The evolution of DNA, chromatin, ribosomes, lipid-membrane-bound organelles, and electron transport chains was also likely to have been decisively influenced by e&. My thanks are due to Professor J. H. Baxendale for discussions.
REFERENCES BALAZS, E. A., DAVIES, J. V., PHILIPS, G. 0. & SCHEUFELE. D. (1968). J. them. Sot. (C), 1424. BAXENDALE. J. H. (1977). Can. J. Chem. 55, 1996. CALVIN. M. (1969). Chemical Evolution. Clarendon Press, Oxford. DAVIES, J. V., DODGSON, K. S., MOORE, J. S. & PHILIPS, G. 0. (1969). Biochem. J. 113, 4651, HART. E. J. & ANBAR, M. (1970). The Hydrated Elecfron. New York: Wiley-Interscience. SCHNECKE, W.. GR~TZEL, M. & HENGLEN, A. (1977). Ber. Bunsenges. phvsik. Chem. 79,475. SHRAGCE, P. C., MICHAEIS, H. B. & HUNT, J. W. (1971). Radiufion Res. 47, 498. STOTT, J. E. (1973). Trans. Biochem. Sot. 1, 787. SCOTT, J. E. (1975). Phil. Trans. R. Sot. London B. 271, 235. SCOTT. J. E., DAVIES, J. V. & EBERT, M. (1975). Trans. Biochem. Sot. 3, 436. WALLACE. S. C. & THOMAS, J. K. (1973). Radiation Res. 54, 49.
Hydrated
19-27
Electrons and Prebiotic Evolution J. E.
Biochemical
SCOTT
Morphology, Department University of Manchester, (Received 20 February
of Medical Biochemistry. Manchester 1979)
It is proposed that reactions of the hydrated electron e, in the “primordial soup” were an evolutionary pressure which selected biopolyelectrolytes. coacervates, “organelles” and lipid-membrane-bound structures of a pattern found in the biosphere today. The two physical restrictions of e, reactivity which determined its evolutionary specificity are (a) its exclusion from polyanion domains in Donnan fashion, and (b) its inability to solvate in alkanes. Thus, (1) polyanions (as opposed to polycations) and (2) lipid-membrane-bound (as opposed to free.) structures are protected from ea.& reactivity and degradation. The polyanionic nature of the current biosphere, and the prevalence of anionic polyanion-polycation complexes (such as ribosomes and chromatin), are attributed to (1). (2) co-operated in protecting the products of (1) as salinity in the “primordial soup” increased and (a) was no longer important. The evolution of DNA, and the existence of electron transport mechanisms are seen as logical extensions of the properties of e, Experimental evidence is already available to support all the postulated processes.
1. Introduction Theories of prebiotic biochemical evolution are necessarily teleological, with the added disadvantage that although the ends may be definable, the beginnings and intermediate stages are not, so that the means are unusually speculative. If it could be shown that given reasonable physical and chemical assumptions, an inevitable sequence of events took place leading to the defined end, this would be widely accepted as proof of the rightness of the assumptions, so small is the likelihood of the contemporary biosphere arising entirely by chance. Miller, Fox, Calvin (1969) and others took the Urey-type planet, with an atmosphere of methane, ammonia, hydrogen and water, as the point of departure, and showed that ambient physical and chemical forces would produce a “primordial soup” containing an enormous variety of monomers 19 0022-5193/79/210019+
10 %02.00/O
0 1979 Academic
Press Inc. (London)
Ltd.
20
J. E. SCOTT
and polymers similar to or identical with present-day biochemicals. How then could this random assortment of building units evolve towards highly ordered “living” systems? This note will show that there was a potent evolutionary pressure which could have led to the selection of a class of polyelectrolytes, and that this selection was an important stage on the route towards the present biosphere. Experimental evidence is available at crucial points. First, it is necessary to identify that aspect of the biosphere which is the goal of our postulated evolutionary process. 2. The Polyanionic
Nature of the Biosphere
A “balance sheet” of contemporary structural biopolyelectrolytes shows a remarkable preponderance of polyanions over polycations (Scott, 1975). Pectins, gums, slimes, alginates, acidic glycosaminoglycans and glycoproteins, nucleic acids, etc., vastly outweigh polycations, of which there are few examples (histones, protamines). The pericellular environment (connective tissue, etc.) is predominantly polyanionic, while polycations are characteristically intracellular, where their properties are not lost in the swamping excess of oppositely charged polymers. This imbalance is not surprising in an oxygen-rich atmosphere, in which polymers would tend to be oxidized, to the point of containing acidic groups as stable end products (Scott, 1975). Although this may be a good reason for the continuance of the current situation, it is difficult to see it as a prime evolutionary,cause, since free oxygen is not a feasible component of an atmosphere containing methane, hydrogen and ammonia. One would have to invoke a mysterious mechanism, arbitrarily timed, to bring about the necessary transition from a primitive to an oxygen-rich atmosphere. A better alternative, and one susceptible of experimental proof, is to look for a factor which was operative before the development of an oxygen-rich atmosphere, which would ensure that the “primordial soup” became enriched in polyanions compared with polycations. The hydrated electron (e,) first described in 1960 appears to be such an agent. It is produced by the action of ionizing radiation on water, or when an electron is released, e.g. by a P-emitting radio-active source, in water (Hart & Anbar, 1970) and is one of the most reactive species known, with a half-life of less than 1 ms. With most organic compounds, it reacts more rapidly, by several orders of magnitude. In the course of reaction with water, etc., it gives rise to other exceptionally reactive species, including H. free radicals (Hart & Anbar, 1970). Although very short-lived, its rapid rate of diffusion (about the same as
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
21
(b)
FIG. 1. Diagrammatic distributions of hydrated electrons (e-) in the electrostatic fields of (a) polyanions and (b) polycations. In (a) the polymer is shielded from the degradative attack of e, and its bye-products, by the Donnan exclusion of e,;, whereas in (b) the polymer backbone is vulnerable, because of Donnan enrichment of the polycation domain in e.; (see Scott, Davies & Ebert (1975)).
the OH- ion), ensures that it is distributed in the electrostatic fields of polyelectrolytes in the same way as other anions, i.e. it is subject to Donnan effects (Scott, Davies & Ebert, 1975). Consequently e, is excluded to a considerable degree from the domain of polyanions (Fig. l), so that the polymer is protected against the chemical reactivity of eti; and its secondary products (H .etc.). The converse is true of polycations, which concentrate e, into their domains (Fig. 1) and are thus especially vulnerable to attack by e, and its products (Scott, Davies & Ebert, 1975). es; cleaves certain bonds (e.g. the peptide bond), and H-is a highly effective degradative species. Other things being equal, polycations would therefore be chemically modified and degraded by e, at much greater rates than polyanions.
22
J. E. SCOTT
FIG. 2. Organic cations and polycations (R+) caught in the domain of a polyanion are protected from attack by e.; which is excluded from the polyanion domain in a Donnan fashion.
Some chemical structures, e.g. alcohols and ethers, are less reactive towards e.& (Hart & Anbar, 1970) and hence polysaccharides are among the more resistant polymers. Polyanionic carbohydrates would therefore be particularly resistant, compared with other biopolyelectrolytes (Scott, 1975). The negative field of the polyanion protects the polymer itself-and it also protects other species caught up within the polyanion domain (Fig. 2). Conclusive evidence is available on this point (Scott, 1975), although the relevant experiments (Balazs er al., 1968) were performed for other reasons. Organic cations (e.g. methylene blue) and polycations (polylysine) react more slowly, by an order of magnitude (Table 2) when present in solution containing an excess of polyanion (heparin) (Balazs et al., 1968a,b). This result is crucial to the theme of coacervate and organelle evolution. The pattern of this experiment (Fig. 2) is precisely that of the nucleic acids, chromatin and ribosomes.In this system, purines, pyrimidines, polycations, polypeptides, and other compounds especially reactive towards e, are protected by a negative field deriving from an enveloping polyanion. Double helical DNA presents an especially clear example. The reactive, vulnerable bases are surrounded by a cage of polyanion, which is itself of the less reactive carbohydrate type. Shragge, Michaels & Hunt (1971) showed that adenine and cytosine are lo-100 times more reactive to e& than corresponding polynucleotides, and particularly double-helical poly (A + U). The formation of nucleic acid complexes of polycations protects the
from
Scott,
Davies
& Ebert
(1975).
2.42 2.68 xx 10’ 10’
0.05 01
phthalate solution
3.7 x 10’ 1.08 x IO8 1.49 x 108
5 mM Polyvinyl in NaCIO,
Cont. of electrolyte (M) 0 OQO5 0.01
Taken
TABLE
1
0.5 mM
1.2 1.14 xx IO8 IO8
24 x tog 3.5 x lo8 2.46 x lo8
Poly-L-lysine hydrobromide in KBr solution
2 mM
Second-order rate constants (m-’ s-l) of ea; u+th polymers
3.1 x IO’
3.9 x IO7 42 x 10’
Polyvinyl-pyrrolidone in NaCIO, solution
5
s
5 ;j m
2 E
fi
z m
2
Data
from
Balazs
sulphate El-’
Ed al. (1968a,b).
47.0
32.0
Protamine 8.5~10-~
orange
0.0
26.0
43.0
M
blue
M
Alone @05
32.0
23.0
M
7.0
3.6
3.5
3.1
0.0 M
Heparin
11.6
17.5
0.05
lo--’ M
E 1-l 0.1 23.0
M
DNA
28.0
2.3
0.0
M
0.7 x 1O-4
E 1-l
TABLE 2 rate constants (1O-4 K, s-l) for the reaction of eO;with organic cations and polycations, alone or in the presence of heparin or DNA
Polylysine hydrobromide lo-“ E I-’
M
Acridine 1o-5
cont.
Methylene 1om5
NaCl
First-order
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
25
polycation from e, (Table 2, Fig. 2). In this way, primitive “chromatin” or “ribosomes” would have been evolutionarily favoured. Salinity is a factor which would have affected the selectivity of ea; as an evolutionary agent. Donnan effects are almost negligible in O-1 M NaCl, and the protective action of the polyanionic field against ea; is minimal (Scott, Davies & Ebert, 1975) (Table 1). The influence of e=; on the evolution of coacervates would have changed completely as the concentration of electrolyte in the “soup” reached isotonic levels. In more dilute electrolyte solutions, ea; and the ambient electrolyte could have collaborated in selecting polyanion-polycation complexes of high stability. Polycation-polyanion complexes are dissociated by salts, at concentrations dependent on the affinity between the interactants (Scott, 1973). Complexes formed through weak interactions can survive only dilute salt solution. At slightly higher salt concentrations the complex dissociates and the free organic cation is subject to the full attack of e&. Appropriate evidence to show this is available (Table 2). Those polyanionic complexes formed via strong interactions would survive the increasing concentrations of dissociative electrolyte and hence also degradative e.;. Specificity in the formation of polycation-polyanion complexes in the surviving “organelles” would be ensured.
3. Oxygen The conditions in which the “primordial soup” developed, viz. slight alkalinity, and an atmosphere transparent to ionizing radiation from space, ensure a high level of e, activity (Hart & Anbar, 1970). Oxygen in the atmosphere would severely restrict it by (a) reducing the level of ionizing radiation falling on the “soup”, because of the formation of the ozone layer, (b) scavenging ea; after its formation, and (c) reducing the pH of the “soup”, following the contingent disappearance of ammonia and the appearance of CO,, etc. in the atmosphere. It is a corollary of the hypothesis that the evolutionary pressure of ea&,practically ceased with the appearance of an oxygen-containing atmosphere. As pointed out above, increasing salinity would have allowed increasingly random destructive effects of e&,, because of the suppression of Donnan effects. The appearance of oxygen in the atmosphere would have effectively stabilized the status quo in the “soup” in terms of polyanion-polycation complexes. This is rather arbitrary, and does not take account of another property of e,, which could further the evolutionary process.
26
J. E. SCOTT
4. Lipid Membranes - in common with most inorganic anions, does not partition from water inzqorganic phases. It does not solvate in, e.g. alkanes (Baxendale, 1977). Thus a lipid layer acts as a barrier to e& movement. It is proposed that soaps, phospholipids and lipids formed enclosed volumes of small dimensions compared with that of the medium, and that the evolved coacervates found shelter from ambient e, within these lipid ramparts. Much evidence is available to show that this is a general phenomenon. Pyrene reacts with less than 2% of its homogenous solution rate when it is present in negatively charged lauryl sulphate micelles (Wallace & Thomas, 1973). In the neutral lecithin micelle it has less than 10yO of its homogenous solution reactivity (Schnecke, Gratzel & Henglein, 1977). Nitroanthracene and benzene show the same pattern of behaviour, serving as models for other reactive structures incorporated into lipid micelles. It is postulated that such “membrane enclosed organelles” evolved to stable organizations, utilizing interactions of the encapsulated coacervates with the inside of the membrane, e&, being the predator responsible for the scavenging of less stable organizations, or “cells”. Further protection for “cellular” structural and informational macromolecules would be derived from the presence of low molecular weight compounds with high reactivity towards e,. By capturing e& such materials would short-circuit the damaging sequence of ea< reactions. In a more advanced form, this mechanism provides a transport sysfemfor e& from the vicinity of the vulnerable macromolecules to the exterior of the “cell” or organelle, showing obvious analogies with contemporary electron transport processes in the mitochondrion, etc. This process, in a model form, has already been shown in the experiments with pyrene solutilized in lecithin micelles (Schnecke, Gratzel & Henglein, 1977). The product of pyrene and e,, a pyrene anion, detached itself rapidly from the micelle in which it was formed into the aqueous medium, where it underwent further reactions. If the pyrene anion (or analogous anionic species) reverted to pyrene in the course of these reactions, it would rapidly be re-incorporated into the micelle, thus completing the electron transfer cycle. In summary, there is compelling evidence that in an environment with a high activity of e,, as the “primordial soup” must have been, a process of selective degradation would have discriminated in favour of polyanions as opposed to polycations; of anionic complexes of polyanions with polycations, as opposed to cationic complexes of the same kind ; and of lipidmembrane-bound coacervates as opposed to free coacervates. The gradual
HYDRATED
ELECTRONS
AND
PREBIOTIC
EVOLUTION
17
increase of salinity with time would have further restricted the range of coacervates which could have survived the attack of e& as well as encouraging aggregation of amphipathic molecules to form membranes and micelles. The simple operation of a cyclic scavenging mechanism for e& within these micelles would have improved the chances of survival of membrane-bound coacervates which possessed it. The evolution of a polyanion-rich biosphere would thus be only the first of several important stages in which e, was involved. The evolution of DNA, chromatin, ribosomes, lipid-membrane-bound organelles, and electron transport chains was also likely to have been decisively influenced by e&. My thanks are due to Professor J. H. Baxendale for discussions.
REFERENCES BALAZS, E. A., DAVIES, J. V., PHILIPS, G. 0. & SCHEUFELE. D. (1968). J. them. Sot. (C), 1424. BAXENDALE. J. H. (1977). Can. J. Chem. 55, 1996. CALVIN. M. (1969). Chemical Evolution. Clarendon Press, Oxford. DAVIES, J. V., DODGSON, K. S., MOORE, J. S. & PHILIPS, G. 0. (1969). Biochem. J. 113, 4651, HART. E. J. & ANBAR, M. (1970). The Hydrated Elecfron. New York: Wiley-Interscience. SCHNECKE, W.. GR~TZEL, M. & HENGLEN, A. (1977). Ber. Bunsenges. phvsik. Chem. 79,475. SHRAGCE, P. C., MICHAEIS, H. B. & HUNT, J. W. (1971). Radiufion Res. 47, 498. STOTT, J. E. (1973). Trans. Biochem. Sot. 1, 787. SCOTT, J. E. (1975). Phil. Trans. R. Sot. London B. 271, 235. SCOTT. J. E., DAVIES, J. V. & EBERT, M. (1975). Trans. Biochem. Sot. 3, 436. WALLACE. S. C. & THOMAS, J. K. (1973). Radiation Res. 54, 49.
