Geophysical and Geochemical Constraints on Molecular ... - RNA World

1 Before RNA and After: Geophysical and Geochemical Constraints on Molecular Evolution Stephen J. Mojzsis Department of Earth and Space Sciences University of California Los Angeles Los Angeles, California 90024-1567

Ramanarayanan Krishnamurthy Skaggs Institute for Chemical Biology The Scripps Research Institute La Jolla, California 92037

Gustaf Arrhenius Scripps Institution of Oceanography University of California San Diego La Jolla, California 92093-0220

1. INTRODUCTION

This chapter offers a description of some of the physical and chemical settings for the origin of life on Earth. Considering the topic of this book, particular attention is given to the conditions for a precursor RNA World; an ab initio system based on phosphate-sugar backbone structures in linear polymers and currently with nitrogen bases as recognition molecules. Both the appeal and the uncertainties in the assumption of an RNA World are obvious. The biochemical advantage of this model has geochemical and cosmochemical complements such as the abundance in the universe of simple aldehydes, “the sugar of space.” With their relatively high oxidation state, the aldehydes are compatible with plausible models of early terrestrial atmospheres dominated by CO2, H2O, N2, and small mixing fractions of CO, CH4 and other reductants. Further suggestions of an RNA World come from observed and inferred sources of active oligophosphates and from concentration mechanisms based on the molecular charge conferred by phosphate esters. Finally, the facile formation of ribose phosphate has been successfully modeled under mild aqueous conThe RNA World, Second Edition © 1999 Cold Spring Harbor Laboratory Press 0-87969-561-7/99

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S.J. Mojzsis, R. Krishnamurthy, and G. Arrhenius

ditions in the laboratory. Obstacles to progress in prebiotic synthesis leading to the inception of an RNA World yet remain. The concentration of neutral molecules such as formaldehyde and glycolaldehyde required to permit the phosphorylation and sugar phosphate formation found in the laboratory remains an impediment to modeling molecular evolution. Furthermore, the oligomerization of nucleosides or nucleotides without the aid of artificial activating groups, and the synthesis and attachment of nitrogen bases in a formaldehyde environment hostile to the stability and uninhibited reactions of hydrogen cyanide, is another complicated problem remaining to be resolved by further laboratory investigations. At least for the time being, these limitations retain the concept of an RNA World as a metaphor in the company of all current theories of the origin of life. This metaphor has, however, several redeeming geophysical and geochemical qualities that may be regarded as strengthening the case for an RNA World as an early phase in the emergence of life on Earth in the earliest Archean (i.e., before 3800 Ma; Ma = 1 × 106 years).

2. EARLY ATMOSPHERE AND HYDROSPHERE

2.1 General Aspects

Because there is no known preserved record on Earth for the state of the atmosphere and hydrosphere during the first half billion years, there remains considerable room for speculation about the nature of this system wherein life began (Fig. 1). It is currently popular to assign early molecular evolution to hot springs or adjacent cooler regions at the surface as in the case of Yellowstone, Wyoming, or at great depth in the ocean as in the case of the submarine hydrothermal or low-temperature vents. The attractiveness of such schemes comes from the conducive environment rich in energy resources that is provided for chemoautotrophs, and from the fact that a few thousand meters of ocean water affords some protection against thermal shocks by meteorites and comets early in Earth’s history (Sect. 4). The appeal also includes the assumption of a hydrothermal supply of organic compounds, suggested by theoretical considerations and laboratory experiments (Shock 1990, 1996; Shock et al. 1997). However, as of today, the analysis of effluents from bioorganically uncontaminated hot or cold springs has failed to show any organic molecules besides methane, perhaps because of insufficient analytical attention paid to this aspect. In contrast, hot springs debouching through sediments transport a variety of organic decomposition and polymerization products, including petroleum,

Constraints on Molecular Evolution

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that are the direct result of thermal breakdown of residual bioorganic matter from past life, now trapped in rocks. A particularly demanding but neglected link in such schemes for biopoesis in hydrothermal vents is the need for a crustal source of reduced nitrogen available for prebiotic chemical reactions, made acute by the low solubility of molecular nitrogen in the water transfer medium. A solution may be found in the mechanism demonstrated by Summers and Chang (1993), showing that photochemically produced nitrite ion is converted to

Figure 1 of life.

Time scale for events with relevance to the origin and early evolution

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ammonia by reduction with Fe++ in solution. The reaction is enhanced in the anion-concentrating reactive mineral green rust (ferroferric hydroxide). In contrast, inorganic carbon and hydrogen in the form of carbon dioxide and water are readily transported into oceanic crust and potentially (but for CO2 not yet demonstrably) reduced there during hydrothermal alteration. The fact that thermophilic Archea are found at the bottom of the phylogenetic tree (Woese 1987) has been considered an argument for the origin of life in a hydrothermal environment. However, present-day Archea are already highly evolved organisms with an elaborate polypeptide-based enzymatic machinery, protecting the otherwise unstable nucleic acid structures against decomposition at high temperature in the immediate vent environment. Though possessing deep phylogenetic roots, these organisms are still very far away from the origin of life. These circumstances tend to induce those advocating these deeply rooted hyperthermophiles as a remnant population from early molecular evolution to retreat from conduits of hot fluid at the vent proper. In the surroundings of hydrothermal vents, temperatures range all the way down to near freezing on the present sea floor, and as low or lower around some continental hot springs in cold climates. Hydrothermal advocates would also be drawn into an accretion camp that places a substantial reservoir of extraterrestrial organic solids, like cometary or carbonaceous meteorite material, in the early crust, available for hydrothermal digestion. If not depending on a source organic compounds from space, much will depend on the outcome of currently intensified analysis of virginal hot spring effluents. Expanded measurements of organic production at hot springs could testify to the efficiency of postulated inorganic–organic reactions. With these provisions and reservations, the hypothesis of hydrothermally assisted molecular evolution would seem to fall within the limits of geophysical and geochemical plausibility. The examples presented here point at the interdependence between different disciplines, and at avenues for verification.

2.2 The “Fertile Atmosphere” and the Concept of a Prebiotic Soup

Already early in the century, considerations of the possible nature of Earth’s primordial atmosphere created compelling arguments for a neutral or weakly reducing composition, dominated by carbon dioxide, nitrogen, and water vapor. In his pioneering electrochemical experiments, Walther Löb (1906, 1914) actually used carbon dioxide and carbon monoxide as major components of the cold plasma discharge system (Fig. 2), which


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Figure 2 Apparatus used by Walther Löb for studying the biomimetic synthesis of organic compounds, including aldehydes (1906) and amino acids (1914) in cold plasmas, with CO2, and NH3 as reactants in various combinations. (A) Plasma generator (“elektrisator”); a, inner tube; b, outer tube; c, plasma discharge space; d, liquid bulb; e and f, three-way stopcocks; (B) burette with leveling funnel; (D), recipient flask for liquid with reaction products; (C) and (E), gas burettes. (Reprinted from Löb 1906.)

was found to produce aldehydes, including glycolaldehyde, and the amino acid glycine. Löb’s experiments were intended as metaphors of the conversion of inorganic carbon and nitrogen to organic compounds by autotrophic life without apparent concern for their prebiotic significance. In contrast, the later and more widely known experiments by Oparin (1924; Oparin and Clark 1959) deliberately aimed at modeling the origin of life. Since the formation of “proteinoids” (postulated then to have been important predecessors of life) demanded a reducing environment, Oparin proposed, without scrutiny of physical plausibilities, that a primordial atmosphere of the Earth must have consisted primarily of a mixture of hydrogen, methane, ammonia, and water vapor. A decisive event in the U.S.

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efforts at scientifically addressing the problem of the origin of life was Harold Urey’s entry into this field after World War II. Although with a better awareness of geophysical limitations (Urey 1952) and unaware of Löb’s biomimetic experiments, Urey nonetheless championed Oparin’s concept of a strongly reducing atmosphere despite objections from contemporary geochemists such as V.M. Goldschmidt (1952) and W.W. Rubey (1951, 1955) as well as organic chemists (Abelson 1966; Ferris and Nicodem 1972). The objections of these and other workers were put into the background by the impressive results of experiments by Miller (1953, 1987; Miller and Van Trump 1981) that expanded Löb’s findings to a plethora of amino acids and other organic compounds forming under fertile Oparin-like conditions. The fact that a variety of amino acids, considered by science at the time to be the initial building blocks in biomolecular evolution, could be formed from a gas mixture with claims for modeling the primordial atmosphere made a lasting impression on organic chemists as well as the general public, and stimulated prebiotic chemistry as a worthy field of study. However, it is now held to be highly unlikely that the conditions used in these experiments could represent those in the Archean atmosphere. Even so, scientific articles still occasionally appear that report experiments modeled on these conditions and explicitly or tacitly claim the presence of resulting products in reactive concentrations “on the primordial Earth” or in a “prebiotic soup.” The idea of such a “soup” containing all desired organic molecules in concentrated form in the ocean has been a misleading concept against which objections were raised early (see, e.g., Sillén 1965). Nonetheless, it still appears in popular presentations perhaps partly because of its gustatory associations. The interest in planetary atmospheric physics and chemistry, rekindled in the era of space exploration, brought physical considerations back into focus in addressing the nature of the early atmosphere. Major contributions to the application of atmospheric dynamics to models for primordial planetary atmospheres were made by Walker (1980, 1982), Kasting and Walker (1981) and later by Kasting and collaborators (Kasting and Walker 1981; Kasting 1982, 1988, 1993; Kasting et al. 1983, 1984; Kasting and Ackerman 1986). These studies again indicated carbon dioxide, nitrogen, and water vapor as dominant components for Earth’s primordial atmosphere and of materials such as H2S, CO, CH4 and H2, ranging in concentration from ppm to a few hundred ppm, as minor components. Melton and Ropp (1958) demonstrated the formation of cyanide ion – by the reaction of atomic nitrogen on HCO2 , reactions that may have taken place in cold plasmas in the Archean atmosphere and ionosphere


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(Sect. 2.3). Atomic nitrogen reacting with small amounts of methane in the upper atmosphere was also proposed by Zahnle (1986) as a potential source for hydrogen cyanide. Subsequent to Löb’s (1906) work, several authors have continued to investigate the formation of aldehydes from CO2, crucial for an RNA World and in what appears to be a realistic vision of the early atmosphere. Modern views have thus returned the atmosphere to only a limited source of strongly reduced compounds for prebiotic synthesis, but still support the production of organic species at the oxidation level of aldehydes. Most importantly, the resulting low concentration in the hydrosphere of organic compounds made available for reaction in a weakly reducing atmosphere has focused the attention on the crucial need for selective concentration mechanisms in models for biopoesis. A related casualty of the organic aridity of a near-neutral atmosphere is the concept of solution in the ocean, taken for granted almost automatically in much of the literature as the site of early chemical evolution toward complex biomolecules. The dilution in the ocean of soluble compounds from any weak source is forbidding; already sparse, unstable molecules introduced in a volume of 1.3 × 109 km3 of seawater are mutually unreactive and hardly retrievable by evaporation or other means. Oceanic boundary reactions at the air–sea or crust–sea interface are entropically more advantageous than anything in the free water column and could have involved, for instance, large-scale processing in the hydrothermal plumbing system of the accumulated polymeric tar that constitutes the major fraction of organics from space. Such matter may have been continuously deposited on the ocean floor in the earliest Archean at a rate some 102–104 times higher than at present (see, e.g., Chyba et al. 1990; Chyba and Sagan 1992). It is conceivable that reactive concentrations of such pyrolysis and hydrolysis products could be maintained in low flow-rate regions of the oceanic crust. Semipermeable membranes of precipitating metal sulfides, observed in laboratory experiments, have been suggested by Russell et al. (1994) as containment for such solutions. Another way to achieve both preconcentration and processing in schemes for biopoesis was quoted by Charles Darwin: a small lake or “pond” with soluble compounds accumulating from a surrounding drainage area. Solar evaporation in a Darwinian pond would be a questionable concentration process in view of the destructive effect of UV radiation on organic compounds. Selective sorption on surface-active sedimentary minerals may be more effective based on experimental results. In such an environment, wide local ranges of pH and temperature could be achieved (Arrhenius et al. 1997).

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A conceptual representation of a number of processes proposed in the literature that could contribute to selective synthesis in the Darwinian environment is schematically illustrated in Figure 3. Extraterrestrial input by proposed higher rates of impact to the early Earth (Sect. 4) is represented by atmospheric ablation of meteors and a cometary impact pond (Clark 1988). Volcanic exhalation products issuing in a glacial environment (Schwartz and Henderson-Sellers 1983, quoting Spitzbergen as a modern counterpart) could be preconcentrated by eutectic freezout in the ice (Sanchez et al. 1966). Oligophosphates condensed in molten volcanic rock have been observed by Yamagata et al. (1991) to be carried into the hydrosphere by supercritical steam and to be effectively concentrated by bilateral surface-active minerals such as double-layer metal hydroxides and clays (Arrhenius et al. 1997). Condensed phosphates may also be produced at contact heating by lava flows over sedimentary deposits containing the protonated Mg-Ca phosphate that is expected as the abiotic product of phosphate precipitation (Sect. 6.1). Surface-active minerals

Figure 3 Physiographic diagram of a “Darwin pond” environment, visualizing proposals made to solve problems in biopoesis by authors referred to in the text. Condensed phosphates are emerging in hydrothermal steam and solution and also produced by lava flows in contact with sediment containing the condensed phosphate mineral, whitlockite, perhaps dominant in an abiotic environment.


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forming from aqueous solution are capable of phosphorylation, selective concentration, and oligomerization of aldehydes and carboxylic acid anions (Pitsch et al. 1995; Kolb et al. 1997; De Graaf et al. 1998). Aside from the accumulation and reaction of prebiotically important organic molecules in lakes, porous groundwater aquifers with slowly diffusing and percolating solutions would offer voluminous and chemically diverse environments for selective concentration and reaction. Such a reacting groundwater environment would be important particularly for relevant chemistry taking place on bilateral surface-active minerals such as doublelayer metal hydroxides and clays. In the “genetic takeover” concept of Cairns-Smith (1975, 1982), this would be the primary medium for emergence of the earliest life forms, with reactive minerals providing an integrated scaffolding, and a part of life itself. The conceptual notions presented in Figure 3 should not be taken too literally from a geographic point of view, but they illustrate principles proposed by various authors in order to overcome some of the important geochemical obstacles perceived in molecular evolution in an Archean environment. 2.3 Synthesis of Source Molecules in the Interstellar Medium and the Atmospheric Electric CIrcuit

The nature of the space medium has increasingly been seen as controlling the production of compounds of prebiotic interest considered difficult to synthesize in an “infertile” terrestrial atmosphere. The favorable conditions for building large organic molecules in the space medium are due to 6 the extremely low kinetic temperatures (10–50 K) and densities ( < ~10 –3 cm ) with resulting long collision lifetimes (hours–days), coupled with high excitation, ion, and electron temperatures (103–106 K). The molecular products of such plasma reactions are gathered in solid condensates and brought to the planets by infalling solids. Such compounds, observed in meteorites, comets, and the interstellar medium, include (in meteorites) ethylene glycol, dihydroxyacetone, glycerol, and glyceric acid (Cooper 1996), hydroxyacids (Peltzer et al. 1984), phosphonates and amino acids (Cronin and Pizzarello 1997), in one case with chiral excess. These all are found in extremely low concentration (ppm range or even less), which emphasizes the problem of bringing these materials to Earth at sufficiently high concentrations for biopoesis. Extended cold plasma regions in the atmosphere include the auroral electrojet (Fig. 4), the subauroral electron deposition region in the upper atmosphere (Fig. 5) and the transient sprites (Fig. 6) and jets in the tropo-

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Figure 4 Electric current structure in the aurora. (Courtesy of C.G. Fälthammar.)

Figure 5

Boreal auroral oval seen from space. (NASA.)


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Figure 6 Red sprite extending above a thunderstorm through the stratosphere and into the ionospheric E-region, forming an electric connection between the ionosphere, the troposphere, and, in the addition to the aurora, a possible mechanism for generation of organic reaction products from cold plasma in a nonoxidizing atmosphere. (Courtesy of D.D. Sentman, University of Alaska.)

sphere-stratosphere. Sprites and jets are luminous transient plasma discharges that, because of the lack of visibility from the ground, have only recently been discovered and explored (Sentman and Wescott 1995; Sentman et al. 1995; Dowden et al. 1996; Hampton et al. 1996). Sprites extend to altitudes of 90–100 km above thunderclouds, forming a link in the atmospheric electric circuit; organic synthesis and transport of products in sprites may have played a role in the upper atmosphere of the Archean. The yield from organic reactions may have been limited by the short pulse duration, which may, however, contribute to efficient quenching of product molecules. In the auroral oval, the currents feeding into and leaving the circuit are powered by the solar wind- magnetosphere dynamo; electrostatic double layers accelerate electrons into the upper stratosphere (3850 Ma, objects believed to be of cellular origin (Fig. 12). The minute dimensions (5–15 µm) of the carbonaceous inclusions require that the mass spectrometric measurements to determine their isotopic compositions be carried out by high-resolution ion microprobe analysis. The stable isotopes of carbon (12C and 13C) are partitioned as a result of both equilibrium exchange reactions and kinetic effects due to the metabolic mechanisms of organisms as well as inorganic processes. Inorganic processes such as evaporation, diffusion, and condensation are of far less magnitude in fractionating the isotopes than biogenically induced fractionations. In the standard delta notation, δ13C is defined as the ratio of the 13C/12C of the sample relative to the ratio of the conventional PeeDee Belemnite (PDB) standard expressed in parts per thousand (per mil): δ13C = {[(13C/12C)sample / (13C/12C)PDB] –1} × 1000. High-resolution mass spectrometric measurements indicate a strong fractionation of 13 12 C/ C (δ13C = –23 to –50%), a range uniquely limited to bioorganic carbon and well separated from the range (around 0–10%), of inorganic sources on Earth (Fig. 13) and in consonance with the bioorganic origin suggested by the phosphate mineral phase association and crystal chemistry (Mojzsis et al. 1996). 7. CONCLUSION: THE WEB OF STRATEGIES

Problems related to biopoesis, the creation of life, are approached in the literature in three stages with growing constraints. At the most fundamental level, an inquiry is made about probabilistic aspects and the generation and transfer of information. Although inspiration at this stage is derived from the chemical structure of the modern replication system, no detailed inferences are necessarily made about structures or reactions participatory in the origin of life; in the words of one of the leaders in the field: “the chemists will take care of that.”

Figure 13 The distribution of carbon isotopic compositions in nature, showing the enrichment of the light isotope 12C by autotrophic organisms (expressed as negative values of 13C). This marked fractionation takes place at the enzymatically mediated transfer from the pool of inorganic carbon (mainly CO2) and identifies bioorganic carbon in fossilized carbonaceous remains of organisms, such as in Fig. 12. Reduced carbon in sedimentary and metamorphic rocks is largely of such organic origin.

38 S.J. Mojzsis, R. Krishnamurthy, and G. Arrhenius


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The organic chemists thus enter at the next stage in the interpretation of what it takes to make life by attempting to identify any stepwise organic chemical process that, coupled with various energy sources, could possibly have led from simple source molecules to complex structures. Such complex structures must have become functionally similar to those active in present-day biosystems. In order not to miss any opportunities at this level, most actors in the origins-of-life field purposely avoid side glances at complicating environmental constraints. Thus, if an appealing but clearly unnatural process is found, adaptation to natural conditions is left behind as a secondary problem to be dealt with downstream. Experimental proof is generally demanded for proposals at this level to be taken seriously. At the third level, the question is raised whether chemically attractive reactions are compatible with environmental constraints imposed by geophysical considerations. Since natural processes are frequently highly complex, and since there is no cohesive geological record from the first 500 million years on Earth, a rather wide latitude for chemical speculation remains yet possible. However, with the combined criteria of the laws of physics and relative plausibilities of geochemical models, in addition to the important and increasing access to planetary materials and the oldest rocks, a more limited set of likelihoods is produced for the conditions present on Earth at the time of the origin of life. A typical example is presented by past chemical theories requiring a high atmospheric partial pressure of molecular hydrogen for desired reactions to proceed. This condition is fulfilled on massive gas-giant planets of the outer solar system like Jupiter. However, the light gases hydrogen and helium rapidly escape from the Earth’s weaker gravitational field, and hydrogen generation sources on a planetary scale, capable of counterbalancing the escape in a sustained fashion, are unknown. We have followed the record of the Archean Earth and prebiotic chemical schemes within the context of early life and the postulated RNA World. We see that the accretion history and early thermal state of the Earth remain subjects of widely varying hypotheses and conjectures, based only on fragmentary observational evidence that provides few concrete constraints. The body of such evidence is, however, increasing, deriving from measurement of magnetization and chemical separation in the interstellar medium, the observation of planet formation around protostars, radiochemical timing of the formation and development of the internal zones of Earth and Mars, and uncovering of increasingly older sedimentary records on Earth. All of these fields are in rapid development based on deliberate research efforts aimed at understanding the early

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Earth and the origin of life. In the present situation it is, however, possible to claim initial thermal states of the Earth ranging from a low average temperature established already during the later stages of accretion, to a planetary ocean of molten magma blanketed by a hot and dense atmosphere, and requiring some kind of corrective acts to convert to a habitable crust and hydrosphere. These events have to take place in time to permit the evolution of biochemically advanced life to appear less than 650 million years after the accretion of the Earth; whether the earliest hints of life so far recognized were part of an RNA World remains unknown. In this situation it is tempting for organic chemists, pursuing all chemically possible but otherwise unrestricted alternatives, to claim that as long as geologists, planetary physicists, and astrochemists cannot make up their minds, and continue to vacillate between such extremes as discussed above, there should be complete liberty not only for exploring all conceivable chemical pathways, but also to claim, without reservation, their validity on “the primitive Earth.” However, as discussed above, additional and much more specific restrictions arise from consideration of the early state of the atmosphere and hydrosphere based on geophysical constraints. This, together with the question of life struggling against all odds in a fragile peace with impacts or other environmental catastrophes in the earliest times brings out the unsolved problem of how much time is needed for life to follow the “cosmic imperative” of de Duve (1995); to emerge from an inorganic state that, according to Descartes “does not act” but merely exists.

ACKNOWLEDGMENTS

The authors acknowledge support from NASA grants NAG5-4563 and NAGW-1031 (G.A.), and National Science Foundation grant EAR9704651 (S.J.M.). Comments on the manuscript by C.E. Salomon are gratefully appreciated. We have benefited from discussions with P.S. Braterman, C.F. Chyba, M. Eigen, C. Engrand, A. Eschenmoser, M. Fayek, H.D. Holland, J.F. Kasting, G. Marklund, L.E. Orgel, and K. Zahnle. We also thank T. Cech for constructive editorial comments, and the invitation to participate in this volume.

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