on the origin and planetary distribution of life

RADIATION RESEARCH 15, 174-192 (1961)

On the Origin and Planetary Distribution of Life'

CARL SAGAN The Institute for Basic Research in Science, The Space Sciences Laboratory,

and The Department of Astronomy, University of California, Berkeley, California

I. INTRODUCTION

The present paper is a discussion of current opinion and speculation concerning the origin and early history of life on Earth, with particular emphasis on the role that radiation may have played, and with application to the problem of extraterrestrial life. The production of organic molecules in the atmosphere and on the surface of the primitive Earth is outlined in Section II, and the origin of the first self-replicating system from these molecules is discussed in Section III. In Section IV the radiation hazards to the first organisms are examined, and possible radiation defense mechanisms and their relation to the early evolution of life are described in Section V. Finally, the application of these concepts to the possibility of life on other astronomical bodies is discussed in Section VI. A more detailed investigation of these and related subjects, especially from the astronomical point of view, will be published elsewhere (1).

II. SYNTHESIS OF ORGANIC MOLECULES ON THE PRIMITIVE EARTH

According to the most successful contemporary view of the origin of the solar system (2, 3), the planets were formed from gas and dust clouds characterized by a "cosmic" distribution of the elements. Astronomical spectroscopy indicates that, with surprising uniformity, the most abundant elements in our galaxy are, in order of rank, hydrogen, helium, oxygen, nitrogen, and carbon. The numerical abundance of hydrogen is in excess one hundred times that of O, N, and C, and it is clear that the most common molecules in cold condensed cosmic objects will be the hydrides H2, H20, NH3, and CH4. The present rarity of the terrestrial noble gases with respect to the cosmic distribution indicates that the primary atmosphere of the Earth was almost completely lost in early times, and that the present atmosphere is of secondary origin (4). The elements which were later to form the secondary

1 Paper presented at the Symposium on Radiation and Space (C. A. Tobias, chairman) at the eighth annual meeting of the Radiation Research Society, San Francisco, May 9-11, 1960.

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ORIGIN AND PLANETARY DISTRIBUTION OF LIFE

terrestrial atmosphere must have rained out of the primary atmosphere in compounds or have been occluded as gases during the formation of the Earth. As the temperature of the newly formed planet increased, owing to the energy of accretion and to radioactive decay, these compounds were decomposed and the occluded gases released. The chemical composition of the secondary atmosphere must at first have been very similar to that of the primary atmosphere. Because of its high rate of escape, hydrogen must have been rather underabundant, and the principal constituents of the atmosphere must have been water vapor, ammonia, and methane. As bodies of liquid water formed, NH3 would go increasingly into solution, and the major nitrogen-containing molecule in the atmosphere become N2 (5). It is this atmosphere of H20, CH4, N2, NH3, and small amounts of H2, and the interaction products of these molecules, which will be called, in the remainder of this paper, the primitive atmosphere of the Earth. The transition from the reducing primitive atmosphere to the present oxidizing atmosphere is attributable to two causes, the photodissociation of water vapor in the high atmosphere with the selective escape of hydrogen, and plant photosynthesis.

There is no accurate and direct determination of the lifetime of the primitive atmosphere, but it seems quite likely that life arose before the transition to an oxidizing atmosphere had been made (see below). The presence of fossilized algae in limestone dated 2.7 x 109 years old (6) suggests that the atmosphere was al- ready oxidizing at that time. Rocks recently dated at 3.4 x 109 years old show ferrous/ferric iron content characteristic of contemporary oxidizing conditions; and it is not unlikely that oxidized rocks with ages approaching 4.0 x 109 years will be clearly identified in the future (J. L. Kulp, private communication, 1961). Thus the primitive reducing atmosphere was in existence for no longer than 1 x 109 years since the stabilization of the Earth's mantle about 4.5 x 109 years ago. There is reason to expect extensive surface remelting and tectonic activity shortly after the stabilization of the mantle. Volcanic environments are probably not ideal for the origin of life. Accordingly, there seems to be at most a few hundred million years for the origin of life on Earth. The event almost certainly occurred 4.0 ? 0.5 x 109 years ago. A more narrowly circumscribed estimate, based on the above remarks, is that life arose on Earth 4.2 ? 0.2 x 109 years ago.

It is now well known that, when an atmosphere of methane, ammonia, water, and hydrogen is irradiated by ultraviolet light, or is sparked by a corona discharge, and the products are allowed to pass into water solution, amino acids and other organic compounds are produced (7, 8). Although corona discharge is a more con- venient laboratory energy source, much more energy was available as solar ultraviolet light than as lightning in primitive times, and from purely energetic considerations it would appear that the bulk of the organic matter produced in primitive times arose from ultraviolet irradiation. However, the newly synthesized molecules often absorb at longer wavelengths than their precursors; since more en-

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ergy is available at longer wavelengths, organic molecules might be expected to be destroyed faster than they are synthesized, and the net rate of photoproduction would be zero. This argument against the effectiveness of ultraviolet organic synthesis was first presented by Pringle (9). It is circumvented if the newly synthesized molecules can travel to atmospheric depths which are opaque in the photolytic ultraviolet before the photodissociating quantum is absorbed. Groth (private communication, 1959) has found that there is sufficient absorption at X 2537 to give amino acid quantum yields comparable to those at shorter wavelengths. Most of the absorption at X 2537 occurs in the vicinity of the relevant unit optical depth. The atmospheric level corresponding to optical depth unity at X 2537 corresponds to greater optical depths at shorter wavelengths. Therefore, only those synthesized molecules which are photodissociated at longer wavelengths than X 2537 will un- dergo photolysis; effectively, this condition permits the photolysis of only aldehydes, ketones, and some aromatic hydrocarbons in the primitive atmosphere. Furthermore, it can be shown that an appreciable fraction of these molecules will escape photolysis through gravitational diffusion (10). Finally, after the development of oceans, when most of the ammonia is near the water surface, convection may be expected to carry much of the synthesized material under the protective cover of the water.

From the quantum yields and the solar ultraviolet flux in primitive times, the net production rate of organic matter can then be calculated (10, 11). For a primitive atmosphere with a lifetime of 109 years, and with no destruction of synthesized material, the total surface density of organic matter at the end of this period is estimated as between 103 and 104 gm cm-2. For comparison, the total quantity of reduced carbon fossilized as argillaceous sediments in the Earth's crust is about 1300 gm cm-2, and the total quantity of carbon fossilized as carbonate is about 3500 gm cm-2 (12). It is consequently tempting to suggest that the carbon of the lithosphere is of ultimate abiological organic origin. In this view, oxidation of primitive organic matter to C02, followed by the Urey equilibrium and the activi- ties of marine organisms, accounts for the present carbonate sedimentary deposits. Some of the reduced sedimentary carbon may be of primitive origin; and it will be interesting to see whether appreciable organic fractions are discovered at the base of the Earth's crust by the Mohole boring. If 103 to 104 gm cm-2 of organic matter were dissolved in the present oceans, a 0.3 to 3% solution would result. This conclusion is in good agreement with the suggestion of Urey (3) that the primitive oceans may have been as much as a 1% solution of organic matter. It is clear that this should provide a very suitable environment for the interaction of the synthesized molecules and the production of organic compounds of high molecular weight.

The identified compounds in the experiments of Miller (7, 13)-the amino and other simple organic acids, urea, and methylurea-comprise about 15% of the total yield. There is some evidence that polyhydroxyl compounds, possibly sugars, were produced by formaldehyde condensation. No purines, pyrimidines, or pyrroles have

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been identified to date. However, hydrogen cyanide and acetylene (13, 14) are known intermediaries in the reactions; and the production of pyridines, pyrimidines, and pyrroles from NH3, HCN, and C2H2 is expected to occur at high temperatures, or by other means of excitation (see e.g., ref. 15). In addition, purines have recently been synthesized abiologically by HCN polymerization (16). The present biochemical precursors of purines, pyrimidines, and pyrroles were available in primitive times. Even without the knowledge of their importance for the origin and history of life, we could have inferred that amino acids, sugars, purines, pyrimidines, and pyrroles were synthesized in high yield on the primitive Earth.

Subsequent interaction of these molecules can be expected to produce a variety of complex organic molecules. Activation energy in primitive times may have been supplied by the penetration of ultraviolet light to the surface, and by radioactive heating. Of the molecules abundantly produced in the gas phase by sparking a simulated primitive terrestrial atmosphere (14), only formaldehyde absorbs strongly at wavelengths greater than X 2400; below A 2400 many molecules begin to have appreciable absorption cross sections. Formaldehyde absorption extends from about A 2900 to longer wavelengths. If such other aldehydes and ketones as acetal- dehyde or acetone existed in fair abundance (>>1 cm-atm), the atmosphere would be opaque between X 2400 and X 2900. But, in the steady state, the amount of such molecules produced in the atmospheric simulation experiments is very low, and the possibility exists that an atmospheric window existed between X 2400 and A 2900 in primitive times. With heat and ultraviolet radiation available at the surface, higher-order organic reactions take place, including the production of polypeptides from amino acids (17-20). It is important to note that since, other factors being equal, complex molecules are better able to preserve their structure after exposure to heat and radiation than are simpler molecules, there is an impetus for the differ- ential survival of the more complex molecules (21, 22). Thus there are two ex- amples of nonbiological natural selection tending to synthesize complex organic molecules on the primitive Earth: the more rapid atmospheric diffusion of higher- molecular-weight compounds to depths which are optically thick in the photodissociating ultraviolet, and the greater resistance of the more complex molecules to pyrolysis and photolysis. Several sites have been proposed for the further accumulation of organic molecules in specific concentration sites, including alumino- silicate clays (23), phase interfaces (24), and coacervates (17). The production of an enormous variety of organic molecules of molecular weight u > 100 must have occurred.

III. ORIGIN OF THE FIRST SELF-REPLICATING SYSTEM It is evident that once a self-replicating, mutating molecular aggregate arose,

Darwinian natural selection became possible, and the origin of life can be dated from this event. Unfortunately, it is this event about which we know least. Because of the central and unique role of DNA in the reproduction of almost all contempo-

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rary terrestrial organisms, it is very reasonable to identify the origin of life with the origin of the first self-replicating polydeoxyribonucleotide (25). The absence of DNA from some plant viruses, where RNA is the exclusive nucleic acid, is not a very strong counterargument, in view of the hypothesis that these viruses are de- generate forms of more complex organisms, lately evolved for a parasitic existence.

A fundamental relevant discovery is the finding by Kornberg that DNA can be synthesized in the laboratory from deoxyribonucleoside triphosphates in the presence of Mg by an enzyme extracted from contemporary microorganisms provided a small amount of DNA is acting as primer (26). Although there is no direct evidence that DNA is synthesized in an analogous manner in vivo, there is strong presumptive evidence that this is the case. It is clear that polynucleotides could not have arisen for the first time in the primitive ocean under precisely these circumstances, because no primer could be available. It is also extremely unlikely that the contemporary polymerase (t > 106) arose spontaneously in primitive times. However, there is one case in which a copolymer of deoxyadenylate and thymidylate is produced by the enzyme in the absence of primer (27); the copolymer then primes the further synthesis of only poly-A-T from a mixture of all four deoxyribonucleoside triphosphates. Since the polymerase only increases the rate of a reaction which must occur in any case, it is possible that the unprimed nucleoside triphosphate polymerization reaction will produce a polynucleotide in times long compared with the duration of the laboratory experiments, but short compared with geological time. The polynucleotide would then serve as primer for subsequent syntheses. Low-molecular-weight polypeptides produced abiologically may have served as primitive polymerases. Since the information-carrying properties of a two-symbol code are evident, the evolution of a primitive poly-A-T is inevitable in a medium containing large quantities of deoxyribonucleoside triphosphates. A specific mechanism for the large-scale production of these precursors in primitive times is needed. A few suggestions on this subject can be entertained, but this aspect of the problem remains largely untouched.

The precursors for contemporary biosynthesis of deoxyribonucleoside triphosphates are formic, aspartic, glutamic, and carbonic acids, glycine, deoxyribose sugar, and phosphates; ATP and a variety of enzymes are also utilized. In primitive times all the precursors were available in great abundance; however, enzyme specificity can hardly be expected, and the presence of ATP is precisely what remains to be explained. Some spontaneous primitive synthesis following present biosynthetic pathways may be expected over long periods of time, but it is unlikely that large quantities of nucleoside triphosphates were produced in this manner. The construction and replication of primitive polynucleotides demand either large quantities of nucleoside triphosphates, or some mechanism for their preferential concentration.

The requirement of deoxyribonucleoside triphosphates for DNA synthesis is

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very interesting in view of the ubiquity of ATP in biological energy transfer. Al- most all biological polymerizations involve the breaking of triphosphate bonds. Blum (28) has proposed that ATP was formed in primitive times and was involved in polypeptide synthesis in the early ocean. If ATP were utilized in primitive polynucleotide synthesis, it is difficult to believe that its energy-transfer potentialities were not similarly utilized. Energy is required for polynucleotide synthesis; for example, in the Watson-Crick model it is required for hydrogen bond lysis. We suggest that the energy is carried by the very nucleoside triphosphates which are incorporated in the new nucleic acid strand. In present organisms the energy carried by ATP is provided by glycolysis and photosynthesis. At the time of the origin of polynucleotides there must have been another energy source. It is noteworthy that purines and pyrimidines have strong absorption bands in the x 2400 to X 2900 window in the primitive terrestrial atmosphere discussed in Section II. We propose that the transferrable energy carried by ATP, and the energy for polynucleotide synthesis, were provided in primitive times by the absorption of solar ultraviolet radiation by these bases near the ocean surface.

Phosphorus plays a unique functional role in contemporary polynucleotide biosynthesis and structure. In addition, it is the only atomic component of polynucleotides which has a relatively low cosmic abundance. To date, phosphates have never been utilized as a component of the liquid phase in the Miller experiments. Such experiments are now planned, and it will be interesting to see whether bio- logically familiar organic phosphates will be produced. The suggestion that the present biochemical role of phosphorus can be traced to its critical involvement in the origin of life (22, 23) is supported by the observations of Fox and Harada (20); they find that the conditions for polypeptide pyrosynthesis are appreciably re- laxed in the presence of phosphoric acid.

IV. RADIATION HAZARDS IN PRIMITIVE TIMES

Various authors have invoked radiation to explain some aspects of the early evolution of life. It is sometimes suggested that high-intensity radiation in primitive times greatly increased the mutation rate, so that an extremely variegated as- sortment of genotypes was presented for natural selection. Such a formulation is an inversion of the problem. In the absence of the carefully controlled environment of contemporary cells, the mutation rate due to errors in copying must have been very high in the earliest life forms. The impediments to their survival must have been so great even in the absence of radiation that large energy fluxes almost certainly would have been lethal. When the mutation rate is sufficiently high, natural selection becomes inoperative, because a characteristic selected for is mutated away too rapidly for it to become established in the population. Present organisms exhibit a mutation rate which is itself depressed by natural selection. High-intensity radiation would pose very grave hazards to the first organisms.

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The time of the origin of life was sufficiently removed from the time of the origin of the elements which compose the Earth that by then most radionuclides had de- cayed to their stable end products. Radio-uranium, -thorium, and -potassium are exceptions, but 4.5 x 109 years ago is only a few half-periods for these elements. Thus the a-, /-, and y-emission from radioactive decay was at most an order of magnitude greater in primitive times than it is today and probably did not play an important role either in the synthesis or in the destruction of organic compounds. The primitive atmosphere was opaque to y- and X-radiation incident from the Sun, and to ultraviolet light of wavelength shorter than about X 2400. There is no reason to assume that the average cosmic-ray flux was very different from today. Krasovskii and Shklovskii (29) have estimated that stars within 5 parsecs of the Sun will become supernovae about once in every 5 x 108 years. Under these circumstances the secondary cosmic-ray flux at the Earth's surface may increase one to two orders of magnitude for a period of about 1000 years, i.e., to about 1 rep year-1. This is unlikely to have important effects at the time of the origin of life. Infrared and microwave radiation either were absorbed by the primitive atmosphere or were transmitted at negligible intensities.

Consequently the radiation hazard problem turns on the intensity of ultraviolet light transmitted in the postulated X 2400 to X 2900 atmospheric window. From models of the evolution of the Sun and an integration of the Planck distribution function, the ultraviolet flux transmitted by an atmosphere containing no aldehydes or ketones other than HCHO is computed to be about 5 x 103 ergs cm-2 sec-1. For a variety of contemporary organisms, chromatid deficiencies or sex- linked lethal mutations in several per cent of the irradiated population occur when doses of about 100 ergs cm-2 at wavelengths between X 2900 and X 2537 are applied to the germ plasm; the mean lethal dose at these wavelengths for many microorganisms lies between 105 and 106 ergs cm-2 (see, e.g., ref. 30). It is observed that the more complex present life forms in general have greater radiation sensitivity than simpler forms, probably because less can go wrong with a simple organism than with a complex one. But it is evident that even the simplest primitive organism would not long survive 5000 ergs cm-2 sec-1 at A < 2900 A. The minimum requirement is that the interval between successive replications be less than the time of accumulation of the mean lethal dose. For an organism replicating, for example, every 104 seconds, with a mean lethal dose at these wavelengths of 107 ergs cm-2, the ultraviolet flux must be less than 1000 ergs cm-2 sec-1 for clone survival. How- ever, unless the availability of deoxyribonucleoside triphosphates and the relevant polymerases was extraordinarily high in the primitive sea, the replication time was very much greater in early times, and the flux must be much less. If we demand that, to avoid excessive mutation rates, the dose per generation be less than 103 ergs cm-2 and assume a replication period of 106 seconds, the incident flux must be kept below 10-3 erg cm-2 sec-1.

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Several tens of meters of water provide an attenuation factor of about 10-7 at these wavelengths and could keep the dose absorbed by the first organisms within tolerable limits. It is likely that the first self-replicating polynucleotides developed in the oceans, and were benthic rather than pelagic.

An accessory problem, however, still remains. It is well-known that ultraviolet light at A < 2900 A absorbed by water produces H202 and such oxidizing free radicals as OH and H02. When ultraviolet light is incident upon a solution of organic matter containing amino acids, organic peroxides are formed by reaction of the amino acids with the photoproducts. It was first found by Stone et al. (31) that ultraviolet pretreatment of the culture medium results in a significant increase in the mutation rate of microorganisms immersed in the medium but not exposed to the radiation. The period of decay of mutagenic activity for organic peroxides at the dilutions mentioned is of the order of 104 to 105 seconds. With present values of oceanic eddy diffusion coefficients, it is easy to show that, at depths of more than about 100 meters, peroxides produced at the surface will have been deactivated before arriving at the bottom of the sea. But by the same token, nucleoside triphosphates and other molecules excited by ultraviolet light at the surface of the prime- val sea will also be deactivated in roughly this period. In order to avoid the more direct effects of ultraviolet irradiation, primitive organisms must have been at least 40 meters below the ocean surface, and benthic. In order to obtain ultraviolet-ac- tivated compounds diffusing from above, primitive organisms must have been at most 100 meters below the ocean surface. But then, a critical problem in the early history of life must have been the presence of mutagenic organic and other peroxides among the molecules photoproduced at the ocean surface and diffusing to lower depths.

V. ANTIMUTAGENIC ADAPTATIONS AND THE ORIGIN OF THE CELL The standard peroxide defense of contemporary cells is catalase. It arises by

adaptive enzyme formation when peroxides are administered to the medium and has the highest specific activity of any known enzyme. In the ultraviolet pretreatment experiments, strains of organisms which ordinarily contained an un- usually high catalase concentration were discovered to be almost immune to the mutagenic effects of both irradiated and hydrogen peroxide-treated media (32). Similarly, catalase inhibitors are found to increase the spontaneous mutation rate (33, 34).

Obligate anaerobes are killed in the presence of molecular oxygen because of the formation of small amounts of peroxides with which they are unprepared to deal. Catalase is absent from many anaerobes; when catalase is administered, these organisms can survive in oxygen (see, e.g., ref. 35 and references given there). Some aerobic microorganisms also lack catalase (36), and other defenses against peroxides-for example, the cytochrome system-must be utilized.

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However, contemporary organisms have a wide range of sensitivities to oxygen and its products, even in the absence of the porphyrins, since some bacteria can survive complete inactivation of catalase and the cytochromes by, e.g., cyanides. This fact has led Molland (36) to conclude that catalase is not necessary for the survival of bacteria today. Such a conclusion would apparently be supported by the observation that, although many enzymes are utilized as food in starving cells, catalase is preferentially metabolized; in the nuclei of starving cells, catalase activity drops to zero (37). Mention should also be made of the interesting discovery by Takahara (38) of an apparently hereditary catalase deficiency in the human circulatory system.

Now it appears very unlikely that a biosynthetic pathway which is relatively easily destroyed by mutation, and which produces an end product of no adaptive value, would not have been lost long ago. It is more reasonable to assume that catalase production is retained because of the consequent depression of the spontaneous mutation rate. On the other hand, it is improbable that such an involved enzymatic reaction chain was developed for such a long-run evolutionary advantage as a lowered mutation rate. We suggest that catalase and similar molecules are relics from primitive times and high radiation environments.

Possible mechanisms for the development of peroxide reduction agents by primitive organisms have been discussed by Granick (39) and by Calvin (40). They have suggested that the selective advantage of such an adaptation was the greater energy available from aerobic metabolism (about a factor of five times as much energy per glucose molecule). But it appears much more likely that the primary benefit of such an evolutionary development was the defense against the mutagenic and lethal effects of peroxides. The aqueous ferric ion catalyzes peroxide reduction, and the simple association of self-replicating polynucleotides with iron would have had great survival potential, and would have been selected. The reason the ferrous-ferric system was selected over other equally efficient systems (e.g., cuprous-cupric, chromous-chromic, titanous-titanic) is simply the much greater abundance of iron, both in the cosmic distribution of elements and in the present distribution in the Earth's crust. It is likely that pyrroles were abundant in the primitive environment (Section II); iron-chelated tetrapyrroles have a thousand- fold increase in catalytic activity over Fe++. Furthermore, in dilute solutions of H202, porphyrins catalyze their own production (40). Combination of proto- porphyrins with protein, forming compounds such as catalase and the cytochromes, increases the catalytic activity by a factor of 1010 over that of the ferric ion. Since each successive step had an obvious selective advantage, and since autocatalysis came into play, it appears likely that porphyrins and catalase were initially associated with primitive organisms as a defense against peroxides. The subsequent utilization of these compounds for electron transfer, autoxidation by 02, sensitiza- tion of water to photodissociation by visible light, and photosynthesis would have

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been later developments. The great variety of fundamental utilizations of these compounds by contemporary organisms points to their early association with life.

It is very significant that oxygen is a poison to the nuclei of all contemporary cells (41). Many aspects of cell physiology, such as the cessation of mitochondrial activity and the induction of a stage of temporary anaerobiosis in normally aerobic cells during division, serve only to prevent contact of the nucleoplasm with molecular oxygen. If the nucleus had developed in an oxidizing atmosphere, these circumstances would be very puzzling; but if it had developed in a reducing atmosphere, the deleterious effects of oxygen and peroxides would be much easier to understand. [Haldane (24), in a similar fashion, argued from the existence of obligate anaerobes, and from the ubiquity of the anaerobic as contrasted with the aerobic glycolytic pathways, that life arose in a reducing environment.] Cells in which nuclear metabolic activity is disproportionately greater than cytoplasmic activity are among the most radiosensitive cells known (42); the reason is essentially that the cytological apparatus for dealing with molecular oxygen and oxidizing radiation products is localized in the cytoplasm and is effectively absent from the nucleus. It is therefore suggested that the cytoplasm was first developed in primitive times to minimize peroxide contact with the nucleus and to deal with the oxygen evolved from peroxide reduction. At a much later time, when the ultraviolet radiation crisis had passed, reaction chains which produce H202 as an end product could be successfully developed.

The physical process which associated polynucleotides with bodies containing porphyrins may have been autocomplex coacervation (43). Such a polynucleotide- porphyrin system must have been far from a recognizable cell. Polynucleotide synthesis was unconnected with division of the entire entity, and enzymatic cataly- sis was very undeveloped. With nucleic acid control of some protein synthesis, perhaps initially because of the corresponding bond distances in polynucleotides and polypeptides, the evolution of biochemical reaction chains can be envisioned along the lines first suggested by Horowitz (44). Synchronization of cell division with polynucleotide replication must only eventually have been selected.

In this view, the evolution of the first organisms was a conservative process. The cell was developed in order to maintain polynucleotide replication without lethal mutation rates. As organisms multiplied and abiologically produced nucleoside triphosphates were depleted from the medium, organisms catalyzed the synthesis of these molecules from precursors, and the first biochemical reaction chains developed. As the number of steps increased, sources of utilizable energy became more important in organizing the syntheses. With plentiful sugars in the primitive environment, the first glycolytic reactions may have developed. In the steady state, the rate of organism replication was directly proportional to the rate of arrival in the sea of photochemically produced organic molecules from the atmosphere. After perhaps 5 x 108 years, however, the photodissociation of water vapor and the

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escape of hydrogen from the high atmosphere oxidized the constituents of the atmosphere, and small amounts of free oxygen were formed. At the same time ozone must have formed by three-body reaction of 02 and 0. On the geological time scale, the appearance of enough ozone to render the atmosphere opaque shortward of A 3000 must have happened very rapidly. But the primary source of energy and material for life was then cut off.

It is evident that only those organisms survived which had evolved from hetero- trophic to autotrophic modes of existence in the period prior to the transition from reducing to oxidizing atmospheres. In the primitive reducing atmosphere, organisms with autoxidizable porphyrin inclusions may have discovered the energetic advantage in utilizing for glycolysis the molecular oxygen released in peroxide reduction. After the transition to an oxidizing atmosphere, organisms adapted for aerobic glycolysis had a selective advantage in the rapidly thinning organic solution. If light were being absorbed by porphyrins, and catalase was abundant as an antimutagen, the evolution of chlorophyll required only a few further synthetic steps. (The suggestion that plastids and mitochondria are closely related even in modern cells dates back to Guilliermond, 45.) Simple photosynthesis, as in the purple bacteria where only acetic acid, light, and some minerals are required, might then have developed. Acetic acid is one of the two most abundant compounds identified in the experiments of Miller and Groth, and its presence well into the period of the early oxidizing atmosphere may be expected. The possible subsequent evolution of photosynthesis, including the origin of carbon dioxide fixation, has been discussed by Gaffron (46).

There is some reason to believe that sexual reproduction developed only after the transition to the oxidizing atmosphere. Today, because of the absence of Mendelian recombination, asexuality involves less phenotypic diversity than does sexuality. On the other hand, asexual reproduction has the selective advantage that genotypes of exceptional adaptive value are not dispersed during replication. But in primitive times, phenotypic diversity was provided by the high mutation rate, and asexuality combined the best features of modern sexual and asexual reproduction. It is expected that any experiment in sexual reproduction was selected against while the mutation rate remained high.

VI. THE POSSIBILITY OF EXTRATERRESTRIAL LIFE

It is likely that the early physical conditions on Earth were similar to the early conditions on the other terrestrial planets, especially Mars and Venus, and the possibility naturally arises that a biological evolution developed on these planets paralleling the evolution which occurred on Earth. In addition, the atmospheres of the present Jovian planets (Jupiter, Saturn, Uranus, and Neptune) resemble the atmosphere of the primitive Earth, and organic molecules are undoubtedly being formed in them today. But before we can evaluate the possibility of extraterrestrial

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life, we must set some boundary conditions on the origin and survival of life. For the present purposes, life is defined as a molecular system capable of mutation and replication. Detailed references to the matters discussed in the remainder of this section can be found in the review of Sagan (1).

Because of their astronomical ubiquity, it is reasonable to expect H, O, N, and C to be fundamental constituents of life on other planets. In addition, these atoms possess properties which seem peculiarly appropriate for the formation of complex molecular systems (see, e.g., ref. 28), including hydrogen bonding and the ability of carbon to form long-chain molecules with variable side groups. Silicon is often suggested, and rarely discussed, as an alternate for carbon. It might be briefly noted here that silicates lack the information-carrying properties of variable side chains which characterize such carbon compounds as polynucleotides and polypeptides. Therefore it is doubtful that silicates could be a fundamental constituent of extraterrestrial organisms. The same objection does not apply to polysiloxanes, but a plausible mechanism for the preferential production of polysiloxanes during early planetary evolution remains to be given.

On bodies with characteristic temperatures less than roughly 400?K, a solvent appears necessary to form complex organic molecules. By far the most desirable substances for this purpose are H20, NH3, and HF, in the liquid phase and in order of desirability (cf. ref. 28). Because of its low cosmic abundance, and for other reasons, hydrofluoric acid seems much less appropriate than ammonia or water. Liquid ammonia is an excellent organic solvent, and on low-temperature planets where it might be available in abundance, analogous systems of organic chemistry should develop, with the NH2 group replacing OH. On bodies with characteristic temperatures exceeding roughly 400?K, and with moderate atmospheric pressures, there would appear to be no appropriate solvent, and the thermostability half-lives of many organic molecules would be so short that familiar organic chemistry would be impossible. Despite the high reaction rates, on the basis of present information the origin of life would appear to be impossible on such high-temperature planets.

A final parameter is time; it is likely that its importance has been overestimated. Although the possibility still remains that the origin of terrestrial life turned on a few very improbable events, the evidence points to a rapid origin of the first self- replicating system (cf. Section II). Therefore it should not be overlooked that life may arise on the planets of rapidly evolving stars, and on planets with rapid temperature evolution owing to the greenhouse effect.

In this solar system, there is convincing evidence for life only on our own planet. But from an observatory on Mars, it is questionable whether even life on Earth would be detectable. Seasonal color variations of cultivated crops and deciduous forests would probably be observable, but varying interpretations of these phenomena would undoubtedly be found. The greatest engineering works would be largely invisible, and the lights of the largest cities would only be marginally de-

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tectable at night. Nuclear explosions would be observable, but their short duration would result in many escaping detection, and almost all evading corroboration. Under these circumstances, it is not remarkable that no convincing direct evidence exists for life beyond the Earth.

Many phenomena observed on Mars have been attributed to indigenous organisms, but alternative interpretations have been proposed, and the issue is far from settled. Early observations of green coloration and rectilinear markings were interpreted as photosynthesizing plants and the artificial waterways of intelligent animals, respectively; this led to the general disrepute of planetary biology among professional astronomers. It is now known that the dominant color of the dark areas of Mars is gray, not green; the green coloration arises primarily from contrast with the buff-colored deserts, and from the chromatic aberration of refracting tele- scopes. Even if green coloration were established on Mars, it would be poor evidence for vegetation. There seems to be no selective advantage for the coloration of chlorophyll, and many terrestrial plants have evolved accessory pigments to absorb in the spectral regions where chlorophyll reflects. Since small changes in the side groups of the chlorophyll molecule have profound effects on its absorption spectrum, it is possible that the green coloration of chlorophyll is largely an his- torical accident. It is unlikely that the same accident would have occurred on Mars. The near infrared reflection spectra of the Martian dark areas argues against a dense cover of chlorophyll-containing plants (2). The apparent rectilinear markings are also largely illusory; under the best seeing conditions with large instru- ments, they are resolved into disconnected fine detail. The canals of Mars seem to be chiefly a psychophysiological rather than an astronomical problem.

In more recent years other observations have suggested that there is life on Mars. The superficial telescopic appearance of this planet naturally separates into three parts-the polar caps, the bright buff-colored deserts, and the predominantly gray dark areas. From polarimetric and infrared spectrographic observations, the polar caps are known to be composed of frozen water, even though the water vapor abundance in the Martian atmosphere is too low for detection from the Earth's surface. The polar ice caps alternately wax and wane; in the Martian spring and fall, water vapor must be in transit between the northern and southern hemispheres. At this time seasonal changes are observed to occur in the dark areas. The outlines of the dark areas sharpen, and their albedo decreases. Predominantly gray areas take on brown or, more rarely, green or blue coloration. Except at the rim of the receding ice cap, these colors-at least in recent years-are delicate pastels. As winter approaches, the outlines become more diffuse, the darkness decreases, and the coloration returns to the predominant gray. These color changes can be attributed to the seasonal growth and decay of Martian vegetation. It has also been suggested that the color changes arise from the response of hygroscopic salts to increased humidity. Although it has been impossible to suggest the precise hygro-

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scopic salts which change color in the appropriate manner at the appropriate humidity, this is not a very convincing objection; after all, no one has described the precise Martian organisms which account for the color changes either. Similar alternative explanations are available for the sharpening of outlines and the darken- ing of areas.

A second seasonal variation occurs in the polarization of the dark areas (47). If the polarization of the dark areas is plotted against phase angle for a given Martian season, a characteristic polarization curve is obtained. The polarization curve for the same areas during a different season has a similar shape but is displaced in the absolute value of the polarization. Curves for the bright areas show no such seasonal variation. In order to reproduce these curves in the laboratory, light must be scattered from small particles about 10-2 cm in diameter. In order to reproduce the seasonal variation in the curves, it must be assumed that Mars is covered with small objects 10-2 cm in diameter which periodically change in diameter, or ab- sorptivity, or both. The polarization data are therefore amenable to an interpretation involving the seasonal proliferation of microorganisms; but it is equally possible that Mars is covered by small nonliving particles which change in size or darkness when the abundance of water vapor varies.

A final observation connected with the possibility of life on Mars is the discovery of absorption features in the 3.4- to 3.7-, range which occur in the reflection spectrum of the dark areas and not of the bright areas (48). These features have been interpreted as vibrational transitions in hydrocarbon and carbohydrate bonds, although the possibility that they arise from a combination of inorganic substances does not seem to have been sufficiently explored. But even by assuming that the identification is correct, the presence of organic matter on Mars is not neces- sarily evidence for life on that planet. It is likely that large quantities of organic matter were synthesized in the early history of Mars, when, presumably, there was both a reducing atmosphere and bodies of water. In the-rather improbable-event that life did not arise, the transition to the present Martitan atmosphere could have occurred with organic molecules still littering the surface. There is no detectable free oxygen on Mars, so oxidation of these molecules would be very slow. The temperatures are sufficiently low that the thermostability half-lives of many organic molecular species exceed 109 years. Consequently, if ultraviolet light is absorbed in the present Martian atmosphere-a matter by no means settled-it is possible that organic matter exists on the surface, but that life does not. How- ever, the localization of organic matter in the dark areas is most naturally explained by a biological origin.

It must be admitted that the evidence taken as a whole is suggestive of life on Mars. The response to the availability of water vapor is just what is to be expected on a planet which is now relatively arid, but which once probably had much more surface water. The physical environment is well within the limits for the survival

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and reaction of organic molecules. The absence of oxygen, relatively low temperatures, and possible high ultraviolet flux are hardly insurmountable obstacles. If the radiation flux is high, it will be interesting to see whether, along the lines of Section V, porphyrins have evolved as antimutagens on Mars. Even if life which was chemically very similar to terrestrial life arose on Mars, subsequent adaptation to the differing environments would have led to great morphological and physio- logical divergences. We should not expect Martian organisms, if any, to resemble familiar life forms. There are several critical experiments which could be per- formed to determine whether life exists on Mars, including observations of possible time, topography, or wavelength variations in the intensity of organic absorption features by a flyby or orbiter; and vidicon microscopy and pH and turbidity moni- toring of deposited nutrient media by a soft lander. Devices to perform such observations are currently being developed by various workers.

Because of its dense cloud cover, the surface of Venus has never been observed. Until Venus landers become feasible, the question of possible habitability of this planet can be discussed only through indirect evidence. The key observation is the 600?K microwave brightness temperature. The most plausible interpretation of this datum is that the emission is thermal and arises from the Cytherean surface. If this is the case, then the prospect of contemporary indigenous organisms on the Cytherean surface is very remote. A consistent interpretation of the high surface temperature can be made in terms of an atmospheric greenhouse effect, dependent on the CO2 and H2O in the atmosphere of Venus (49, 50). If carbon dioxide and water-or their precursors-were exhaled from the interior at slow rates, the surface temperature would have increased only gradually from the equilibrium radiation temperature of an airless planet with the albedo and solar dstance of Venus, viz. about 250?K if the period of rotation is much less than the period of revolu- tion. Temperatures could have been low only when there was very little water; the possibility that life arose in the distant Cytherean past is accordingly rather remote.

Customarily Mars and Venus are considered to exhaust the possible habitats of indigenous organisms in the Solar System. But it is becoming increasingly clear that other bodies may hold considerable interest for problems of the origin of life and of extraterrestrial biology. Complex organic matter has now been detected in carbonaceous chondrites (51), and it has been suggested that all chondrites, the most abundant variety of meteorite, arise from carbonaceous chondrites (52). The presence of organic matter and indigenous organisms on bodies such as the Moon is no longer so improbable as was once thought to be the case, although these prospects still remain remote (11, 53). Other objects of renewed serious interest are the Jovian planets.

From atmospheric simulation experiments, it is clear that simple organic molecules must be produced in the atmospheres of the Jovian planets by solar ultra-

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violet light or atmospheric electrical discharges (14). From ultraviolet light alone, the production rate of organic molecules per unit area on Jupiter exceeds the meteoritic deposition rate per unit area on Earth. The Jovian atmosphere is known to be convective, and these molecules will be carried below the visible cloud layer. Now the amount of methane and ammonia spectroscopically identified above the cloud layer will be essentially opaque in the far infrared part of the spectrum. If Jupiter has a surface which is opaque to visible light, this surface will be heated by light penetrating through the cloud layer and will emit in the infrared. But because of the absorptive properties of the atmosphere, this infrared radiation emitted from the surface will be unable to escape to space, a very efficient greenhouse effect will be established, and the temperature of the Jovian atmosphere will increase sharply with depth below the visible cloud layer. It is possible that temperatures near room temperature or above prevail deep in the atmosphere of Jupiter. From cosmic abundance considerations, there must be water on Jupiter; there is no mechanism for its preferential escape during the process of planetary formation. The standard explanation of the absence of spectroscopically detectable amounts of water is simply that it is frozen out; the temperature of the cloud layer is ap- proximately 140?K. But if warmer temperatures prevail beneath the cloud layer, the possibility arises that water or ammonia seas exist on Jupiter. Organic molecules produced in the atmosphere would be carried downward and dissolved in solution, and complex prebiological organic reactions could take place. If this pic- ture is correct, these processes have been operative for the last several billion years on all four Jovian planets. At the present writing, the possibility of life on Jupiter seems somewhat better than the possibility of life on Venus.

There are two important prospects for further knowledge about the origin of life and its prevalence beyond the Earth. One is a continuation of the laboratory work initiated within the last decade to simulate possible primitive conditions and preferentially synthesize the components of self-replicating molecular systems. Further investigation of the mechanisms of molecular self-replication in contemporary organisms will approach the same problem from the opposite direction in time. The second prospect is the possibility of experiments carried by planetary flybys, orbiters, and landers to detect extraterrestrial life. The synthesis of life in the laboratory, or the discovery of life beyond the Earth, cannot fail to have the most profound influence on human thought and action.

ACKNOWLEDGMENTS I am grateful to Drs. N. H. Horowitz, J. Lederberg, S. L. Miller, and H. J. Muller, and to L.

Sagan for stimulating discussions on some of the topics covered in this paper. The production of this paper was supported by the Panel on Extraterrestrial Life, Armed Forces-National Re- search Council Committee on Bio-Astronautics, National Academy of Sciences, and was per- formed in part at Yerkes Observatory, University of Chicago. RECEIVED: February 2, 1961

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