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Planetary environments and the origin of life.

As a consequence of advances in modeling planet formation processes, Earth is now thought to have formed hot, rather than cold, with core formation occurring during accretion. The atmosphere and oceans formed early, and although the climate was probably hot early on, the variation of surface temperature over time is largely unknown. Depending on the redox state of the mantle and that of impacting bodies, the atmosphere could have been weakly or strongly reducing overall, with perturbations caused by impacts. Seawater composition and redox state would have been governed primarily by circulation through hydrothermal systems. Out of this planetary context, life emerged at least 3.85 billion years ago (1), less than 600 million years after the period of planetary accretion.

Equable conditions for prebiotic evolution could have existed as early as 4.4 billion years ago. But these conditions were interrupted by major short-term perturbations in surface environments caused by a declining flux of impactors. Although giant impactors undoubtedly constrained the timing of life's origin, quantitative statements about when the clock was set await a stronger consensus on impactor fluxes and more refined theoretical models. Organic matter that survived impacts or was synthesized in impacts would have augmented the inventory of compounds produced endogenously in surface environments (2). But the fate of organic matter in large ([greater than]1 km) projectiles is poorly understood, and all estimates of the survival or synthesis rates from such impacts are highly uncertain [ILLUSTRATION FOR FIGURE 1 OMITTED]. At the other extreme, impactors in the 10-50 [[micro]meter] range (interplanetary dust particles), derived from comets and asteroids, would have decelerated gently in the upper atmosphere and are thought to have provided a substantial flux of organic matter early on (3).

The geological record indicates the presence of carbon dioxide in the atmosphere as long ago as 3.8 billion years, but it is mute with respect to methane or carbon monoxide. If organic matter had to form in the atmosphere, theory and experiment indicate that productivity in atmospheres dominated by carbon dioxide would have been orders of magnitude lower than in those dominated by the reduced gaseous forms of carbon [ILLUSTRATION FOR FIGURE 1 OMITTED]. If the atmosphere has been only mildly reducing since the end of the major epoch of accretion at [approximately]4.4 Ga, the apparent lack of strong atmospheric sources of hydrogen cyanide, formaldehyde, and ammonia poses a serious challenge for theories of prebiotic evolution, which require these key chemical intermediates for synthesis of more complex organic compounds (4). While the oxidation state of the prebiotic atmosphere remains controversial, little question exists about the reduced state of the early ocean. Only recently, however, have researchers begun exploring its potential for organic synthesis.

Environments at phase boundaries between gas, solid, and liquid states would appear to be highly favorable for prebiotic evolution and the origin of life, provided that they contain suitable sources of energy. These criteria are met by marine hydrothermal systems, intertidal regions, and the wind mixed layer of the ocean. These regions are ubiquitous, geophysically active boundary regions far from equilibrium, with gradients in properties maintained by physical and chemical energy fluxes. Within these environments, small-scale interfacial regions are provided by aerosols, volcanic and extraterrestrial dust, hydrothermal minerals, chemical precipitates, and vesicle-like structures of organic or mineral chemical composition. Inasmuch as life itself must have emerged as a phase-bounded system, the ability of an environment to form, dissipate, and reform small-scale interfaces (structures) must have been a prerequisite for the origin of life. In any such locale, however, there must be processes that offset the hazards of dilution, burial, and secondary decomposition of the compounds which are destined to be the molecular building blocks of life.

Decades of laboratory experimentation have been devoted to demonstrating steps in the prebiotic synthesis of the precursors of proteins, nucleic acids, and membranes. Yet, many uncertainties - about the monomers that were necessary and the manner of their production - remain. These uncertainties persist in some measure because most model syntheses suffer from dubious geochemical plausibility. The bulk of this work has also been carried out within the context of a canonical scenario for a stepwise progression toward the origin of life, from simple reactive compounds, to monomeric building blocks of proteins and nucleic acids, to the biopolymers themselves, to replicating systems. The validity of such a scenario has been largely accepted on faith, and alternatives merit experimental and theoretical exploration.

Literature Cited

1. Mojzsis S., G. Arrhenius, K. D. McKeegan, T. M. Harrison, A. P. Nutman, and C. R. L. Friend. 1996. Evidence for life on Earth before 3,800 million years ago. Nature 385: 55-59.

2. Chyba, C. F., and C. Sagan. 1992. Endogenous production, exogenous delivery, and impact-shock synthesis of organic molecules: an inventory for the origins of life. Nature 355: 125-131.

3. Anders, A. 1989. Pre-biotic organic matter from comets and asteroids. Nature 342: 255-256.

4. Chang, S. 1993. Prebiotic synthesis in planetary environments. Pp. 259-299 in The Chemistry of Life's Origins, J. M. Greenberg et al., eds. Kluwer Academic, Dordrecht, The Netherlands.


YARUS: You have said that the reductive scenario might be rescued, but put in jail. That is, it might apply for short times, following certain impacts. What are those impacts? Are they at all probable?

CHANG: My response to your first statement is, "Yes." But "held captive" is probably a better term. "Held captive," probably, until more information is available on how the interior of the earth works. That has to do with how long, if ever, the early earth was able to maintain an atmosphere that was in equilibrium with metallic iron in the upper mantle or the core. A second point to consider is the prospect that some impactors were iron asteroids, or that the surface rock of the early earth still contained metallic iron during the prebiotic evolution era. In both cases the hot gases added to the atmosphere by vaporization of projectile and target during hypervelocity impact would have been substantially reduced. The carbon originally in these materials would have been converted to carbon monoxide. The larger and more iron-rich the projectile, the larger the amount of carbon monoxide that would have been generated. It is likely that much of the iron in earth's core was derived from iron-rich asteroids, and impacts with such objects must have continued after core formation since we continue to recover iron meteorites today. Those are the possibilities if organic synthesis must take place in a reduced atmosphere. On the other hand, I suggest that organic synthesis need not take place in the atmosphere. Drs. Wachtershauser and Shock (1, 2) would like to convince you that considerable organic synthesis can take place in hydrothermal systems. However, that issue is not resolved.

ELLINGTON: In your presentation, it seemed you were implying that polymer catalysts arose prior to polymer replication. Where do you think polymer replication fits in with the evolution of catalysis?

CHANG: I'm not sure that I believe that polymer catalysis was important. Perhaps catalysis was important, but catalysis can take place without polymers. Short oligonucleotides and short peptides can be catalytic. In addition, the very surface of a membrane may be catalytic. Catalysis has to emerge before polymer replication. One might even argue that polymer replication is preceded by oligomer replication, and oligomer replication can then evolve chemically in conjunction with the evolution of catalytic function. I think that the development of catalytic functions and of the information system needed for replication is a single process. I believe the replication system is an emergent property of catalysis which may have its beginnings at the level of short oligomers.

GUERRERO: In your presentation, you showed the presence of a subsurface biosphere. I see this as a critical issue. We now know that microbes live in granite and in basalt at a depth of 2 km, which implies the possibility that life occurs at these depths on other planets. Before we recognized microbial life at these depths, we were limited to the "photosphere," the well-lit surface of the planet. We know high pressure can be tolerated. The possibility of the origin of life in the deep subsurface, at high pressure, and in the absence of light from any star has increased. This changes our scenarios.

CHANG: I don't disagree with you. I think that the hydrothermal systems are especially interesting and that the subsurface systems are somewhat less interesting. From my perspective as a physical organic chemist, I think we will finally discover that the organisms inhabiting subsurface biospheres never arose there, but rather colonized those extreme environments. If that is true, then I'm not sure that the granitic or basaltic subsurface environments are particularly interesting for the origin of life. On the other hand, those subsurface systems do appear to have liquid water and a continuous source of energy: hydrogen and C[O.sub.2] are present and can be coupled.

Literature Cited

1. Wachtershauser, G. 1988. Before enzymes and templates: theory of surface metabolism. Microbiol. Rev. 52: 452-484.

2. Shock, E. 1992. Chemical environments of submarine hydrothermal systems. Origins Life Evol. Biosphere 22: 67-107.
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Title Annotation:includes discussion; Evolution: A Molecular Point of View
Author:Chang, Sherwood
Publication:The Biological Bulletin
Date:Jun 1, 1999
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