The Origin of Life in the Solar System: Current Issues

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THE ORIGINOF LIFE IN THE SOLAR SYSTEM:Current Issues

Christopher E Chyba White HouseFellow, National Security Council~Old Executive Office Building, Washington DC20506 Gene D. McDonald 2 Scripps Institution of Oceanography,University of California, San Diego, La Jolla, California 92093

I can see no other escapefrom this dilemma(lest our true aim be lost for ever) than that some of us shouldventure to embarkon a synthesis of facts and theories, albeit with second-hand and incompleteknowledge of someof them--and at the risk of makingfools of ourselves. Erwin Schr0dinger, What is Life?

INTRODUCTION Progress in the study of the origins of life was dramatic during the decade of the 1980s. Primordial Earth was put morecompletely into the context of early Solar Systemhistory, and as this planetary view provided newinsights, other by Stanford University Libraries on 04/23/05. For personal use only. Solar Systemenvironments took on greater interest as points of comparison. Workon the energy sources needed to synthesize organic monomersor more sophisticated products on prebiotic Earth expandedwidely, with a numberof provocativenew ideas vying for attention. But mostimportantly, the elucidation Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org of a putative RNAworld held out the hope for resolution of long-standing difficulties in the origin of DNA-proteinorganisms. This reviewis intended to report on someof the current issues in origins-of- life and exobiology research. Wetherefore cannot hope to present a compre- hensive history of the subject. For such reviews, the reader is instead referred

lThe ideas contained in this article do not necessarily represent the views of the National Security Council or the United States Government. ZCurrent address: Laboratory for Planetary Studies, Space Sciences Building, Comell University, Ithaca, NewYork 14853. 215 0084-6597/95/0515-0215505.00 Annual Reviews www.annualreviews.org/aronline

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to Loomis(1988), Or6 et al (1990), and Mason(1991). A compilation original papers has recently been provided by Deamer& Fleischaker (1994). Finally, Shapiro (1986) offers a skeptical review of just howincomplete our understandingof this subject remains. The review consists of four sections. To a great extent, the sections are independent of one another and maybe read in almost any order. Wefirst examinetwo areas of general relevance to exobiology: the definition of life, and the existence of possible extraterrestrial environmentsfor life in our Solar System.We then focus on two areas of morespecific interest to the origin of life on Earth: possible energy sources for prebiotic chemistry, and the RNA-world hypothesis. Wehave not hesitated to draw attention to topics that we think require renewedattention, even if these are not nowthe focus of majorresearch efforts or conferencesessions.

DEFINITIONS OF LIFE

Thereis a kind of ennui that arises over efforts to provide an encompassingdefi- nition for life. Manyattempts have been made;Sagan (1970) has reviewedphys- iological, metabolic, biochemical, genetic, and thermodynamicdefinitions, and there have been manyothers. It is nowa commonplacethat the various proposed definitions virtually all fail: Onecan devise either counterexamplesof systemsthat fit this or that definition, but whichare not generally considered to be alive, or counterexamplesof organismsthat are clearly alive, but which a particular definition seemsto exclude. Crystals, fire, automobiles,and mules are well-known examples of these problem phenomenaand organisms. A sure indication that this definitional frustration has becomepart of the zeitgeist was the depiction in the popular novel The AndromedaStrain (Crichton 1969) the futility, if not hubris, of scientists trying to arrive at a completedefinition.

by Stanford University Libraries on 04/23/05. For personal use only. Claiming this or that counterexample to be an "unimportant" exception implicitly invokes further criteria in addition to those ostensibly comprising the definition. Either a counterexamplefalsifies a particular definition, or we need to be willing to say, for example,that a muleis not a living creature, or

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org that a crystal is alive. Why,then, resume that debate here and now--or for that matter, anywhere or ever? There are two good reasons. There is nowone workingdefinition for life that is becomingwidely accepted in the scientific community.Moreover, there has been a proliferation of artificial systems,both in the laboratoryand in the computer,that comeinterestingly close to satisfying this definition.

DarwinianDefinitions The definition of life that is becomingincreasingly acceptedwithin the origins- of-life communityis essentially the "genetic" definition, e.g. "a systemcapable Annual Reviews www.annualreviews.org/aronline

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of evolution by natural selection" (Sagan 1970). A recent careful formulation, given by Joyce (1994a,b), is: "Life is a self-sustained chemicalsystem capable of undergoing Darwinianevolution." The most important ambiguities in this definition are: Whatexactly is meant by "self-sustained" and "Darwinian"? Joyce (1994a) explains: "The notion of Darwinian evolution subsumes the processes of Self-reproduction, material continuity over a historical lineage, genetic variation, and natural selection. Therequirement that the systembe self- sustainedrefers to the fact that living systemscontain all the genetic information necessary for their ownconstant production (i.e. metabolism)." Note that the use of the adjective "chemical" in the definition given above, whichwe henceforth call the "chemical Darwinian"definition, excludes computer"life" by fiat. The chemicalDarwinian definition excludes biological viruses as well, by virtue of the "self-sustained" requirement. McKay(1994) also accepts the genetic definition, defining life to be material system that undergoesDarwinian evolution." This means, he writes, "that it is capable of self-reproduction, and mutation followed by selection based upon stored information." Whenspecificity is required, we refer to this definition as the "material" Darwiniandefinition. It does not a priori exclude computer"life." Darwiniandefinitions have becomequite influential, shaping not only our views of what life is, but also of howwe define its origin. The viewthat "the origin of life is the sameas the origin of (Darwinian)evolution" is becoming commonplace. Thepopularity of the chemicalDarwinian definition has no doubt been fueled by the breakthrough of the "RNAworld" (Gilbert 1986, Joyce 1991; also see the RNAworld section below). Prior to the discovery of that possible world, the origin of life was faced with the chicken-or-eggparadox of metabolismvs genetic information, whichled someto separate the origins of the two functions. In that sense, adopting the vocabulary of Dyson(1985), there could

by Stanford University Libraries on 04/23/05. For personal use only. have been two separate "origins of life," the first of metabolism(possibly capable of reproduction without replication), the second of replication (see also Morowitzet al 1988). With the discovery that one molecule, RNA,could serve both functions, being both phenotype and genotype, the Darwiniandef-

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org inition nowseems more certain to embracethe relevant historical phenomena. Of course, Earth’s peculiar history need not correspondto the history of life elsewhere. The metabolic vs genetic dichotomy has led to two disparate approaches to origins-of-life research and to two approaches to life’s definition: One path emphasizesthe primacy of metabolism, the other of genetic information [Kamminga(1988) has reviewedthe history of these approaches]. To the extent that speaking of a "metabolism"carries connotations of compartmentalization (e.g. as in Dyson1985 or Morowitzet al 1988), the two approaches remain distinct. However,"metabolism" need not require compartmentalization, Annual Reviews www.annualreviews.org/aronline

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What is metabolism? Kiippers (1990) defines metabolism in the context of the thermodynamicrequirements of life. Because of the Second Lawof Thermodynamics,a living system can only remain alive if the production of entropy is offset by an input of energy or energy-rich matter. Metabolismis then no morethan the turnover of free energythat makesit possible for a given system, compartmentalizedor not, to avoid reverting to an equilibrium state of maximumentropy. In this sense, the chemical Darwiniandefinition of life includes both genetic and metabolic components.

Compartmentalization The Darwinianview of life does not require compartmentalization;an evolving system of naked RNA,for example, might well satisfy the definition. How- ever, the emphasison proteins and nucleic acids has largely overlooked the important role that membranestructures play in life on Earth. The unit of all contemporarylife (assumingthe exclusion of viruses) is the cell, and an obvi- ous function of the cell membraneis to maintain macromolecularcomponents within an enclosed microenvironment,preventing the diffusion of these components into the surroundingmedium while allowing for transport of nutrients and waste products. In a prebiotic setting, compartmentalizationcould provide a mechanismby which systems of diverse macromoleculescould be maintained, leading to encapsulatedexperiments in the origin of life. Historically, the origin of boundedmicroenvironments has received some attention. Oparin (1924) proposedcolloidal coacervates as a possible model. Fox & Harada (1958) argued for proteinoid microspheres. However,contemporarycell membranesare not colloidal or proteinoid in nature, but are based on lipids. Deamerand his colleagues (Deamer& Pashley 1989) have shownthat amphiphilic molecules (molecules that self-assemble into bilayer aggregates

by Stanford University Libraries on 04/23/05. For personal use only. owingto their polar and nonpolargroups; lipids are one type of amphiphile)are present in the Murchisoncarbonaceous meteorite. Moreover,at least one class of these moleculeshas the ability to self-assemble into membranousvesicles. It seemspossible, then, that such vesicles wereavailable on the prebiotic Earth.

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org For the genesis of primitive cellular life, such vesicles would somehowhave encapsulated (Deamer& Barchfeld 1982) both metabolizing and information- bearing molecules.This scenario remindsus that a particular ingredient (in this example, a boundary membrane)might have been essential for the historical terrestrial origin of life, but remaininessential to the abstract definition of life, or even its creation accordingto that definition.

Never since Darwin There are important drawbacksto Darwiniandefinitions of life, as Fleischaker (1990) has emphasized:"Any definition of the living that includes ’the capacity Annual Reviews www.annualreviews.org/aronline

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to evolve’ is doublyproblematic because such a definition requires not only the future state of a single system but other systemsas well." Individual sexually reproducing organisms in our DNA-proteinworld do not evolve. Worse, from an operational point of view, it mayprove impossibleto tell whethera candidate system satisfies the Darwiniandefinition. Howlong do we wait for a system to demonstrate Darwinianevolution? Howdo we tell whether it is or is not capable of this, and under whatconditions? Apositive result is informative; a negative one mayprovide little information. These apparent dilemmascan be largely defused by recognizing that we are actually discussing two distinct, though clearly related concepts: "life" and "a living entity." The Darwiniandefinition refers to a system that implicitly contains morethan one individual entity. Fleischaker’s "system," by contrast, comprisesa single individual candidateliving entity. She presents a definition of an "autopoietic system"that is an operational definition for a living individual. In her words, "Whereas’autopoiesis’ defines an individual living system by its organizationat the present moment,’evolution’ characterizes ’life,’ a single collective phenomenonthat exists over time." Fleischaker’s (1990) proposeddefinition is determinedby three criteria. The living entity must be: 1. self-bounded, 2. self-generating, and 3. self- perpetuating. Withoutdwelling on the details of her definition, we note that she intends it to allowus to identify either the emergenceof life, be it historically in the Archeanor experimentally in our laboratories, or the existence of extraterrestrial life. Thedefinition is meantto haveoperational utility for a single organism, if need be. Fleischaker’s definition wouldacknowledge that Victor Frankenstein(Shelley 1818)created li ving entity inthelab,but that singular creation was not "life" by the Darwiniandefinition.

Life in the Laboratory by Stanford University Libraries on 04/23/05. For personal use only. There are nowa numberof laboratory systems of self-replicating and "evolving" molecules that comeclose to satisfying the chemical Darwiniandefinition of life (see e.g. Achilles &vonKiedrowski 1993, Beaudry& Joyce 1992, Lehman

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org & Joyce 1993, Bartel & Szostak 1993, Joyce 1993, Rebek 1994a,b); Orgel (1992) has recently presented a review. There are at least two respects in which certain of these systemsmay not yet satisfy the definition. For example, the RNAsystems of Beaudry & Joyce (1992) or of Bartel & Szostak (1993) involve amplification (i.e. replication) via the polymerase chain reaction(PCR) or related procedures. The use of modernbiochemical machineryviolates the requirement of the chemical Darwiniandefinition that life be genetically self-sustained. Thesystem does not contain all the genetic information necessary for its ownproduction; rather, one or more enzymes, not coded for by the RNAmolecules being replicated, are required in the amplificationstep. For any particular system,it remainsan interesting question, Annual Reviews www.annualreviews.org/aronline

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however, to ask whetherthe enzymesused merely increase the rate of chemical reaction that wouldhave occurred even in their absence. In that case, it would be less clear that the "self-sustained" requirementwas actually being violated. In Rebek’s(e.g. 1994a,b)self-replicating system, on the other hand, no additional enzymesare required. In someof these experiments,a type of selection is driven by irradiation with ultraviolet light (Honget al 1992). Of course, humanintervention was required to set up Rebek’sultraviolet source. For that matter, the componentsof Rebek’s molecules are human-engineered(e.g. the molecules are predesigned to "mutate" upon exposure to the specific wave- length generated by the UVsource), and replicate in a thoroughly contrived nonaqueous solvent. But nowherein the chemical Darwinian definition are limitations placed on the nature of the specialized environmentin which the candidate life-form must evolve. These wouldbe additional criteria, extrinsic to the definition, reflecting no morethan prejudices about what is "natural." The world is full of organismswith extremely specialized environmental requirements. The Darwinian definition does not care. Rebek’s system passes the "self-sustained" requirement, as do von Kiedrowski’s(e.g. von Kiedrowski 1986, Terfort &vonKiedrowski 1992, Achilles &vonKiedrowski 1993), which also managetheir replication in the absence of an enzyme. Admittedly,these systems, relying as they do on synthetic chemists to provide the systemwith specific starting materials, do not providea realistic simulation for the prebiotic origin of life (and in fact were never intended to do so). But this, too, is an ambiguityfor all prebiotic experiments. The Miller-Urey experiment (Miller 1953, 1974), based on a methane-ammoniaatmosphere, was once considered to have provided an excellent simulation of the early Earth environment.Now, however, it is suspected (see e.g. Walker1986) that this reducing atmosphere maynever have existed; the early atmosphere may instead have been composedmostly of carbon dioxide. If so, Miller’s starting

by Stanford University Libraries on 04/23/05. For personal use only. ingredients mightalso be depicted as artificial. Thesesorts of assessmentsmay be relevant to a judgmentof howaccurate a given experimentis as a simulation of early Earth; they are not relevant to the Darwiniandefinition. Onthe other hand, there are clearly ambiguities with the phrase "capable

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org of undergoing Darwinian evolution." For example, von Kiedrowski and his colleagues (von Kiedrowski et al 1991, Terfort &vonKiedrowski 1992, von Kiedrowski 1993, Sievers &vonKiedrowski 1994) argue that the replication exhibited to date by laboratory systems does not satisfy a certain requirement that is implicit in the phrase "Darwinianevolution?’ Darwinianevolution, which they take to be synonymouswith "survival of the fittest," is said to meanin the laboratory that "the most efficient replicator outgrowsits less efficient competitorsand finally supersedes themin the reaction chamber"(von Kiedrowski 1993; see also Eigen & Schuster 1979). This is distinct from result in whichthe most efficient replicator is unable to entirely outcompete Annual Reviews www.annualreviews.org/aronline

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its less efficient competitors in a struggle for commonresources, so that all replicators survive(i.e. continueto reproduce)at different but equilibriumlevels of concentration ("survival of everybody"; SzathmLry1991). Szathm&y Gladkih (1989) have shownthat subexponential growth in a system of self- replicating moleculesmust lead to this type of coexistence (see also Szathm~y 1991). Current laboratory self-replicating systems exhibit only subexponential (typically parabolic) growth(von Kiedrowskiet a11991, von Kiedrowski1993), so are not yet capable, by this definition, of Darwinianevolution. Further examinationof the putative identity of the concepts"survival of the fittest" and "Darwinianevolution" wouldhelp clarify this issue.

The Ghost in the Machine The preceding discussion about contrived laboratory environmentsfor living systems is directly relevant to discussions of computer life. (For reviews of progress in computer life, see Langton 1992 and Levy 1992.) While the chemical Darwiniandefinition excludes computerlife, the material Darwinian definition speaks only of a "material" system, leaving the door open. In a "functionalist" view (e.g. Sober 1992), Darwinianevolution is a process that can be abstracted from whatever particular physical details are necessary to realize this process in a given system. It is not the computerthat is said to be alive, but the processes themselves. The material substrate of the computer is a humancontrivance that makesthese processes possible, but it is a con- trivance whosestatus is no different fromthe glasswareand chemicalsolutions required for artificial laboratory life. It seemsunsurprising that, in this view, "living" systems or ecosystems can be created in a computer(e.g. Rasmussen 1992, Ray 1992).

by Stanford University Libraries on 04/23/05. For personal use only. Is a Complete Definition Impossible ? A completedefinition for life wouldprovide criteria that were both necessary and sufficient for an entity to be called "alive." Kiappers(1990) has arguedthat

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org such a definition is inconsistent with a reductionistic, i.e. a physical, basis for biology. The premise that life can be explained completely within the frame- workof physics and chemistryrequires, he asserts, that the transition fromthe nonliving to the living be a continuous one. A completedefinition, one that unambiguouslyseparated nonlife from life, wouldonly be possible if the transition fromthe first to the secondwere discontinuous. "However, the definition would then inevitably contain at least one irreducible concept, which would express the ontological difference betweenliving and nonliving systems. Since this conceptwould by definition be life-specific, every holistic definition of ’life’ mustbe inherently tautologous,"he states. "It is thus an absolutelychar- acteristic feature of physically oriented biology that it cannot give a complete Annual Reviews www.annualreviews.org/aronline

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definition of the phenomenon’life.’ If such a definition existed, this fact would contradict the premisesof the reductionistic program,"Kiippers concludes. Whateverits other merits or demerits, it is a virtue of the Darwiniandefinition that it belies this conclusion. Onecan imagine, for example,a transition from nonlife to life on early Earth that would have been discontinuous, such as a discrete changein a particular RNAmolecule that suddenlygave that particular moleculethe ability to self-replicate, initiating a system undergoingDarwinian evolution. Thelatter conceptis "life specific" in the sense that it is central to the definition, but it is not "irreducible"; it is readily elucidatedby a behavioral description that need not refer tautologously to life. Whilethere wouldhave been at least somesatisfaction in concludingthat a completedefinition of"life" was impossible, it seemswe are denied even that consolation.

EXOBIOLOGICAL ENVIRONMENTSIN THE SOLAR SYSTEM In the previous section, we discussedpossible definitions of "life," and definitions of "a living entity." In principle, an accepted definition of life could be applied to newphenomena discovered during the exploration of extraterrestrial environments, to determine whether this or that newly discovered system was alive. But in the absence of samplesreturned to Earth for extendedlaboratory analysis, it is hard to imaginedefinitions as abstract as those discussed above being of practical use in planetary exploration, even given very sophisticated instruments. This is likely to be true even for Fleischaker’s "operational" definition. Whatis neededis a remotely operational definition. Sucha definition wouldmake no pretense of being completeor universally applicable, but would have the advantageof utility in a remote-sensingcontext. Lederberg(1965) suggested a variety of possible criteria that couldbe applied remotelyto the question of life on Mars,including a search for optical activity by Stanford University Libraries on 04/23/05. For personal use only. and the detection of informational macromolecules.But Lederberg noted the dangers in these approaches; remarkingthat biochemistry had then only barely reachedthe point of demonstratingthat the ubiquitous antibody x-globulin had

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org an informational sequence specified by a polynucleotide, he wrote that this ignorance "must evoke somehumility in our postulations and experimental efforts concerning macromoleculeson another planet?’ A decadelater, the Viking landers on Marsconfirmed this dilemmaof extrap- olation. Results from the Viking biology packages(Klein 1978, Margulis et al 1979, Horowitz 1986) were powerful reminders that supposedly unambiguous characteristics of terrestrial biology could crumblein the face of unanticipated extraterrestrial chemistry. Did Viking discover biology or only exotic chemistry? Had the Viking gas chromatograph-mass spectrometer (GCMS)not demonstratedthe absence of organic moleculesto the level 10-6 to 10-9 at the two Viking landing sites (Biemannet al 1977), the ambiguity might never have Annual Reviews www.annualreviews.org/aronline

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been resolved (Cooper 1980). Indeed, some membersof the l,~king biology teamcontinued to argue for a biological explanationof certain results, despite the GCMSdata (Levin & Straat 1981). Of course, it is in principle possible to send remoteinstruments that are less .theory-laden in their interpretation than were the experiments in the Viking package. A possible example of such an instrument would be a microscope; Lederbergoutlined the advantages of that instrument in life remote sensing experimentsas early as 1960 (Lederberg1960). Nevertheless, even this instru- mentcould pose difficult problemsof interpretation in a remotesensing context. A numberof authors have described the difficulties in distinguishing between terrestrial microfossils and nonbiologicalstructures, and the criteria that may be applied to determinewhether putative microfossils are actually of biological origin (e.g. Schopf& Walter1983, Strother 1992). Makingthis distinction for living systems,rather than microfossils, couldbe easier, as living systemsmight have the advantageof motility or other distinguishing characteristics. But there is no reason whythis would necessarily be the case, especially on the time scales available to a practical experiment. Moreover,distinguishing between microscopiclife and microscopicnonlife in a thoroughlynovel extraterrestrial microworldcould provide ambiguities that we cannot nowimagine. Again, this is the lesson of Viking. At this stage in the exploration of our Solar System,it maybe that all the criteria so far discussedremain too ambitiousto be useful in a search for life. McKay(1991) has suggested that, as a matter of practicality, it is wisest developcriteria for the possibility of life "basedon a very conservativeanalysis of terrestrial biology." This analysis notes the importanceof an energy source and a handful of commonelements, especially, of course, carbon. But the sine qua non of life as we knowit is liquid water. Even given an abundance of the necessaryelements and copioussunlight, terrestrial life absolutely requires

by Stanford University Libraries on 04/23/05. For personal use only. liquid water (Mazur 1980, Kushner 1981, Horowitz 1986). This would also appear to be the lesson of the dry valleys in Antarctica, the harshest desert on Earth with virtually no signs of life outside of specific, protected habitats (McKay1986, Campbell & Claridge 1987).

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org Froman operational point of view, then, McKay(1991) argues that the search for life elsewherein the Solar Systembecomes the search for liquid water (see also Chang1988). Weshall apply this criterion to weighpossible habitats for life elsewherein our Solar System,but first note howthis differs fromanother, well-knownperspective in exobiological investigations. The assumptionmade in McKay’soperational definition is that searching for life meanssearching for life as we knowit. Suggestions of drastically different life forms (such as life based on silicon rather than carbon), he asserts, lie in the realm of uncon- strained speculation, and therefore have "not madesignificant contributions to exobiology." Annual Reviews www.annualreviews.org/aronline

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This is quite distinct fromthe view, moststrongly associated with Sagan(e.g. 1961, 1974), that warnsthat attempts to generalize from the single exampleof life of which we have knowledgeare fraught with danger. "In our present profoundignorance of exobiology,life is a solipsism," he writes (Sagan 1974). "There is no aspect of contemporarybiology in which we can distinguish the evolutionary accident from the biological sine qua non. Wecannot distinguish the contingent fromthe necessary." Parochialismis the great danger in looking for life as weknow it. It is possible life maylook nothing like what weknow. Nor are discussions about alternative foundations for biology doomedto no morethan speculation. The assumption that extraterrestrial biology would, after all, be based on someform of chemistry allows somespeculations to be weighedand foundwanting. Morethan three decades ago, for example, Sagan (1961) noted that "silicates lack the information-carryingproperties of variable side chains which characterize such carbon compoUndsas polynucleotides and polypeptides. Therefore it is doubtful that silicates could be a fundamental constituent of extraterrestrial organisms." Nevertheless, speculations about radically different extraterrestrial biologies are hard-pressedto offer search strategies for life on other worlds. In practice, proponentsof both viewpoints wouldagree that our greatest chance for success is to look wherewe are most likely to find liquid water. McKay(1994) concludes that "Whatis needed moredata points, not moreimagination." In lieu of imagination,then, let us examinea range of possible exobiological habitats in our ownSolar System, using the requirementthat liquid water may nowbe (or once havebeen) present as a criterion that has to be met for a location to merit consideration.

Mars--Then and Now Marsremains the center of attention for those hoping to find life elsewherein by Stanford University Libraries on 04/23/05. For personal use only. our Solar System. [See Horowitz(1986) for a critical review of the history these hopes.] Theresults of the Viking biology packageseem best explained as the results of oxidant chemistry, not biology (Klein 1978, Marguliset al 1979),

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org and the observedabsence of organics at the two landing sites (Biemannet al 1977)may suggest that the surface of the planet is nowsterile (Horowitz1986). Theorigin of Martiansurface oxidants is at least partly understoodas a natural result of photochemistryin the atmosphere(Hunten 1979); this in turn implies that the oxidants are globally distributed. Nevertheless,laboratory experiments with terrestrial organisms(Mancinelli 1989) do not support the claim that the Martian surface wouldtherefore be "self-sterilizing" and utterly inhospitable to life. In any case, an oxidizing surface layer wouldonly extend to a finite, possibly quite shallow, depth (Bullock et al 1994). Organicmaterials reported in a Martian-originating meteorite (Wright et a11989)suggest that organics may indeed be present on Mars, although subsequentanalyses indicate that most or Annual Reviews www.annualreviews.org/aronline

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all of this organic carbonis terrestrial contamination(McDonald & Bada1995). All the same, liquid water cannot nowexist on the Martian surface (Carr 1981, McKayet al 1992), which by McKay’soperational criterion suggests we must look elsewherefor life. If life ever did exist on Mars,it is possible that it retreated to subsurface niches associated with hydrothermalactivity, whereliquid water mayexist. Bostonet al (1992) have consideredthe existence of a deep subsurface microbial ecology on Mars, similar to those knownto exist on Earth at several-kilometer depth in oil fields, aquifers, and other locations. Morebroadly, Gold(1992) has speculatedthat Earth is hometo a "deep, hot biosphere"in the terrestrial crust, not dependenton solar energy, and comparablein biomassto surface life. If life could originate at depth, independentlyof surface conditions, such deep biospheres could be widespreadamong the planets and larger moonsof the Solar System.(The possibility of an origin of life at terrestrial hydrothermalvents is discussedin the next section.) If, however,life requires specific surface conditions (such as solar energy) to originate, extensive deep biospheres wouldonly exist--if they exist at all--on worlds wherethe surface was once hospitable. It is hard to see howto pursue these speculations with respect to Marsor other worldswithout first better exploring the extent of subsurfacelife on Earth. Could life have originated on Mars? There is a great deal of geomorpho- logical evidence that water, in the form of groundice, exists at or near the Martian surface (Squyres & Carr 1986, Squyres 1989a). Extraterrestrial water in the Mars-originating SNCmeteorites provides laboratory evidence for Martian water (Karlsson et al 1992, McSween& Harvey 1993), as does the presence of water-precipitated minerals in these meteorites (Gooding1992). Earth obtained a substantial fraction of its oceansfrom cometary impacts, these collisions should have contributed to the Martian water inventory as well, although this conclusionis complicatedby the problemof impact erosion (Melosh & Vickery 1989, Chyba1990a). by Stanford University Libraries on 04/23/05. For personal use only. It is also clear from Marinerand Viking imagesthat this water once flowed at the surface (Carr 1981, McKay& Stoker 1989), probably pooling in lakes (Goldspiel & Squyres 1991). Geomorphologicalevidence for the existence

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org early Martian oceans (Baker et al 1991) has been presented, though this claim remainscontroversial. It appears that Marsbegan as a wet, but not necessarily muchwanner (Squyres & Kasting 1994), world (Squyres 1984, Pollack et 1987), but then evolved into a frozen desert. Mars’ early, more hospitable conditions roughly coincided in time with the origins of life on Earth (McKay 1986, McKay& Stoker 1989), and it appears that liquid water habitats could have been maintainedunder ice covers on Marsfor as long as 700 million years after meanglobal temperaturesfell belowfreezing (McKay& Davis 1991). It natural to ask, if life beganin liquid wateron early Earth, wouldlife have simul- taneously evolved in a similar climate on early Mars? Answeringthis question Annual Reviews www.annualreviews.org/aronline

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requires a search for ancient Martianmicrofossils. The difficulties associated with demonstrating the biological origin of putative microfossils (Schopf Walter 1983, Strother 1992)--or fossil stomatolites (Walter 1983)--in terrestrial rocks warnus that this search mayprove extremelydifficult. Althoughthe difficulties faced by traditional schemesfor panspermiaare well known(Davies 1988), it is possible that microorganismscould have migrated betweenEarth and Marswithin debris ejected fromthe vicinity of large impacts (Melosh1988, see also Moreno1988). There is nowexperimental evidence that impactscan eject a small quantity of lightly shockedmaterial at high velocity (Gratz et a11993,Melosh 1993). To provide an effective vehicle for panspermia, such ejecta wouldhave to be in the form of boulders large enoughto provide shielding fromcosmic rays during the transit times of millions of years required to travel betweenthe two worlds(Melosh 1988). If fossil evidenceis ever found for life on ancient Mars, it mayprove very difficult to determinewhether this life originated on Marsindependently of Earth, or whetherMars was inoculated by microorganism-richmaterial fromterrestrial impacts. Similarly, it is not out of the question that Marscould instead have inoculated the early Earth.

Jupiter and the .Giant Planets Sagan& Salpeter (1976) have presented possible ecologies for organismsliving aloft in the Jovian atmosphere.Similar niches might exist on the other gas gi- . ants, especially Saturn. Clearly these ideas are extremely speculative. McKay (1994) has objected that there are no knownairborne ecologies on Earth, a planet whoseatmosphere is, he states, moreclement and energy-rich. (Note, however, that the reducing atmospheresof the giant planets ensure a continual production of organic molecules.) Whyaren’t the clouds green? Perhaps airborne envi- ronmentson Earth are simply too short-lived, with fallout times too short to permit colonization by microbes. Similarly, on Jupiter, organismswould face by Stanford University Libraries on 04/23/05. For personal use only. the peril of descendingto levels wherepyrolysis wouldoccur. Evenif buoyancy mechanismsto avoid this fate can be envisioned (Sagan & Salpeter 1976), the chancesfor originating life under such conditions are very difficult to assess. Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org Europa The Galilean satellite Europamay be the most intriguing potential exobiological environmentin the Solar System. Tidal heating calculations indicate that Europacould have a deep (> 100 km)ocean of liquid water beneath its fractured (but, judging by the virtual absence of impactcraters, very young)icy surface (Squyres et al 1983). If such an ocean exists, calculations based on Antarctic microorganism analogues show that there could be regions on Europa with physical conditions lying within the range of adaptation of terrestrial organisms (Reynolds et al 1983, 1987). The key question remains whether Europa Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 227

does or does not have oceansof liquid water; radar sounding(Squyres 1989b) the upcomingGalileo spacecraft’s exploration of the Jovian system could possibly settle this issue. Observationsof geysers of ice crystals and vapor would provide dramatic evidence for a second liquid water ocean in our Solar System.

Titan Titan, the large moonof Saturn, presents a prebiological organic chemistry laboratory on a planetary scale. With its N2atmosphere containing several percent CH4,production of complexhydrocarbons and other organic molecules occurs throughthe action of ultraviolet light andradiation chemistry(Sagan et al 1992). However,the low surface temperatures preclude the existence of liquid water, whichargues against the presence of life. Nevertheless, recent work on the formation of transient liquid water environmentsby impact cratering (Thompson& Sagan 1992) suggests that prebiological "experiments" involving high concentrations of organics in the presence of liquid water have occurred on Titan throughoutits history. Thecrater-floor pools of liquid water resulting fromthese impactsare calculated to have characteristic lifetimes of-~103years.

Comets Spacecraft missions to comet Halley have confirmedpreencounter suggestions that cometsare rich in organics; Halley appears to be ~25%organic by mass and perhaps 40-50%water ice (Delsemme1991). With cosmic abundanceratios mostelements, all the ingredientsfor life are certainly present. In the absenceof liquid water, however,comets appear to be poor environmentsfor life (Bar-Nun et al 1981). Thelack of life on Earth’s Polar Plateau and Greenlandice sheet suggests to Huebner& McKay(1990) that the far-less-hospitable environment comet ice should be similarly lifeless. Nevertheless, Hoyle & Wickramasinghe

by Stanford University Libraries on 04/23/05. For personal use only. (1987, 1988a,b) and Wallis et al (1989) have argued, on the basis of compar- isons of the 3.4 micronspectral feature in cometHalley with that of mixturesof viruses and bacteria, that comets are rich in microorganisms.These cometary organisms,they believe, are responsible for the outbreak of various epidemics Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org in humanpopulations (Hoyle & Wickramasinghe1979, 1991). These claims have been counteredby any numberof specialists in the various relevant fields (see Marcus& Olsen 1991 for a review). In particular, the 3.4 micronfeature cometaryspectra is readily explicable by the presence of abiological organics (Chyba& Sagan1987, 1988). Both that feature and its predicted heliocentric evolution (Chybaet al 1989) are increasingly well understoodas a combination of gas-phase and solid-state features (Mummaet al 1993). The possibility of life on cometsturns on whetherliquid water cores exist in cometarynuclei. Our progress in answeringthis question has recently been summarizedby Podolak & Prialnik (1994). The key requirements for melting Annual Reviews www.annualreviews.org/aronline

228 CHYBA& McDONALD

to occurat the center of a cometarynucleus are a large nuclearradius, a low thermalconductivity, and the initial presenceof sufficient aluminum-26to provide substantial heating throughradioactive decay. Recentobservations makeit clear that manygiant comets(radii > 100km) exist (see Weissman1994 for a summary);26Al-heating could possiblysustain liquid cores in cometsof this size for as longas 109 years(Irvine et al 1980,Wallis 1980). If life could originate in the absenceof solar radiation, suchcometary environments would be excellentcandidates for extraterrestrial habitats. However,our knowledgeof the cometarynucleus remains too poorfor any firm conclusionsto be reached concerningthe existenceof liquid cometaryinteriors (Podolak& Prialnik 1994), muchless about "deep"cometary biospheres.

As~mids Speculationabout the origin of life on planetesimal-sizedbodies has focusedon comets,perhaps because they are so water-and organic-rich, but also perhaps in part becausethey remainsufficiently poorlyexplored and mysteriousthat speculationfaces fewconstraints. In this context,it is striking that so little currentattention focuses on asteroidsas potentialsites for extraterrestriallife, especially since wehave in our collections numerousmeteorites (most of whose presumptiveparent bodies are asteroids) that showdirect evidenceof having experiencedorganic synthesis in the presenceof liquid water. Perhapsone reasonfor the relative lack of attention nowgiven to meteorite parentbodies as potentialabodes of life is the acrimonioushistory surrounding early publishedclaims for discoveriesof microfossilsand other biogenicmate- rials in meteorites.This debate began in the early 1960sand continuedfor about a decade;reviews of this controversyinclude those by Urey(1966), Rossignol- Strick & Barghoorn(1971), and Day(1984). There seemsto be a consensus that the "organizedelements" found within certain carbonaceouschondrites are by Stanford University Libraries on 04/23/05. For personal use only. a combinationof terrestrial contaminantsand nonbiologicalmineral or organic structures(Day 1984), providing no persuasiveevidence for extraterrestriallife. Yetby the operationalcriterion suggestedat the beginningof this section-- the presenceof liquid water---certainmeteorites (and their presumptivepar- Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org ent bodies)provide us with the onlyextraterrestrial examples,besides ancient Mars,where this criterion is, or oncewas, fulfilled. Thereis ampleevidence for preterrestrial aqueousalteration in meteorites,both from mineralogy (Zolensky & McSween1988, Grimm& McSween1989) and from the aminoacid and hy- droxyacid profiles of carbonaceouschondrites, which suggest that they formed by the Strecker mechanism,requiring liquid water(Peltzer et al 1984, Cronin 1989, Kerridge1991). Theliquid waterenvironment on the parent bodyof the CI chondriteOrgueil is constrainedby strontiumisotopic evolution to have occurredvery early, certainly within108 yr, andpossibly within 107 yr, of its formation(Macdougall Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 229

et al 1984). Modelsof the thermal history of asteroids suggest that "-,100-km radius asteroids could have maintainedliquid water interiors for several hundred million years (DuFresne& Anders1962, Scott et al 1989), reasonablyconsistent with the empirical results. However,Peltzer et al (1984) determinedthat the time required for the Strecker synthesis on the Murchisonmeteorite parent body could have been as short as 104 yr. It is temptingto use carbonaceouschondrites as indicators of the extent of chemicalevolution that can occur in the liquid water interior of a planetesimal- sized object. Timescales of ~108yr for the duration of liquid water environments in meteorite parent bodies are comparableto the time scales thought to have been available on early Earth for the origin of life, given the likely constraints imposedby impact"frustration," i.e. sterilization of the surface (Sagan 1974, Maher& Stevenson 1988, Oberbeck& Fogleman1989, Sleep et al 1989, Chyba1991). If the Orgueil parent body had in fact contained liquid water for l0s yr, that meteorite could present a primafacie case that prebiotic organic evolution in planetesimal interiors simply does not go very far. Unfortunately, it is unclear that this conclusionapplies to the moreorganic- and water-rich interiors of comets. Giventhe uncertain time scale of Orgueil’s liquid water history, it is even unclear to whatextent this conclusionapplies to other asteroids, and in any case the meteorite sampleavailable to us appears not to be representative of the overall asteroid population(Lipschutz et al 1989). The monomersfor biomolecularsynthesis and potentially catalytic clay minerals have been identified in carbonaceouschondrites, whereevidence of liquid water also exists. Organic componentsthat form membrane-likevesicles have also been extracted from Murchison(Deamer & Pashley 1989). Yet abiotieally produced polypeptides or oligonucleotides have not been reported. Cronin (1976), searching for small peptides in Murchison, concluded that no more than 9 mol%of the total acid-labile amino acid precursors in the meteorite werepeptides. The relevant reaction rates or productionefficiencies in this en- by Stanford University Libraries on 04/23/05. For personal use only. vironmentmay be so low that even a Murchison-sizemeteorite does not contain detectable amountsof abiotically produced biomacromolecules.Perhaps this meansthat liquid water, prebiotic monomers,and mineral catalysts are together insufficient for further progress towardthe origin of life in a time span of 107- Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org 108 years. If so, whatadditional crucial ingredient did ArcheanEarth have that the sampledmeteorite parent bodyenvironments did not? Surely this is a question of great interest for understandingthe origin of life on Earth (and, perhaps, its possibility on comets). Still, it maybe prematureto concludethat chemical evolution in meteorite parent bodies has not progressed past the monomerstage until a thoroughsearch of meteoritic samplesfor prebiotic macromoleculeshas been made, ideally using modernhigh-sensitivity methods. Nonetheless,if the search for life in the Solar Systemis the search for liquid water, we have found it, or at least its dry remains. Althoughthe samplesize Annual Reviews www.annualreviews.org/aronline

230 CHYBA& McDONALD

is far too sparse to draw general conclusions, our first limited experiencewith extraterrestrial liquid water environments,possibly of substantial duration, so far does not reveal progress far downthe road towardslife.

So far we have discussed possible Solar Systemenvironments for life, as well as criteria for recognizinglife shouldit inhabit any of these. However,the only place in the Solar Systemwhere we knowthat the origin of life has actually occurredis on Earth. Wenow turn to two current issues in the study of the origin of life on Earth: the sources of energy available to drive prebiotic organic synthesis and the possible role of nucleic acids or their analogs as the first biomacromolecules.

ENERGY SOURCES FOR PREBIOTIC CHEMISTRY The importance of various energy sources to prebiotic organic synthesis in a planetary environmentis intimately related to the oxidation state of that environment. For the early Earth this is uncertain, and argumentsbased on cos- mochemicaland geochemical principles for both reducing and nonreducing environmentshave been reviewed extensively (Changet al 1983, Walkeret al 1983, Walker1986, Hunten1993, Kasting1993, Kasting et a11993). In this section we discuss recent workon several possible sources of energyfor prebiotic organic chemistry on the ArcheanEarth. Wefocus on the production of several basic prebiotic molecules: nitriles such as hydrogencyanide (HCN),aldehydes such as formaldehyde(H2CO), amino acids, purine/pyrimidine bases, and carboxylic acids (Figure 1).

Atmospheric Energy Sources by Stanford University Libraries on 04/23/05. For personal use only. Atmosphericorganic chemistry on the early Earth has been one of the major thrusts of origin-of-life research duringmost of its history, and the relative importanceof the several available energysources (ultraviolet photolysis, electric

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org discharges, shock synthesis from thunder or bolide impacts, and charged par- ticle radiation) in prebiotic atmospheresof varying compositionsis relatively well understood. A review of the theoretical and experimentalwork in this area is beyondthe scope of this article; the reader is referred to recent reviewsof this subject (Changet al 1983; Ferris & Hagan1984; Or6 et al 1990; Chyba Sagan 1991, 1992; Chang1993).

Exogenous Delivery The origins of life on Earth coincided with the final throes of the heavy bom- bardmentof the inner Solar Systemby cometsand asteroids (e.g. Chyba1993). Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 231

H CH3--C--COOH CH3(CH2)nCOOH I NH2

Aminoacid (Alanine) Carboxylicacid

NH2 O

Adenine Guanine

O 2NH

0 0

Uracil Cytosine

Figure1 Structuresof a typicalamino acid, a carboxylicacid, andthe four basespresent in RNA--thepurines adenine and guanine and the pyrimidinescytosine and uracil. by Stanford University Libraries on 04/23/05. For personal use only.

The diameter-frequencydistribution of lunar craters makesit clear that the bulk of mass collected by Earth during the heavy bombardmentwas concentrated in the largest impactors. Of these, cometsare by far the most organic-rich bodies, Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org containing HCNand H2COat a level "~10-3-10-2 relative to H20 (Mumma et al 1993). Simulations of cometarycollisions with Earth strongly suggest that organic moleculeswould not survive these collisions (Chybaet al 1990), althougha large cometarycollision could lead to a transient, hot atmosphericen- vironmentwith a high abundanceof excited chemicalspecies whosesubsequent quenching could favor synthesis of organics (Or6 1961, Oberbeck& Aggar- wal 1992). Experimental simulations of such syntheses (Mukhinet al 1989) have not unambiguouslydistinguished between surviving organic fragments of the original material and post-vaporization recombination, and are therefore difficult to interpret (Chyba& Sagan1992). Annual Reviews www.annualreviews.org/aronline

232 CHYBA& McDONALD Interplanetarydust particles (IDPs),which are "--10%organic by mass,are another possible importantexogenous source of prebiotic organics (Anders 1989). In an intermediateoxidation-state atmosphere,IDPs could have been the dominantsource of organics on prebiotic Earth (Chyba& Sagan1992). However,the organics in IDPs are poorly characterized and seemlikely to consist primarilyof kerogen-likematerial. Lasermicroprobe techniques have recently demonstratedthe presenceof polycyclic aromatichydrocarbons, or PAHs(Clemett et al 1993). Therelevance of IDPs to early prebiotic syntheses will remainunclear until further compositionalanalysis canbe carried out, a task that is difficult becauseof the smallquantities of materialinvolved (Gibson1992). Themost dramatic data point for the exogenousdelivery ofprebiotic organics to Earthis the discoveryof twoextraterrestrial aminoacids, ot-aminoisobutyric acid and racemicisovaline, immediatelyabove and belowthe clay layer marking the Cretaceous-Tertiary(K/T) boundary (Zhao & Bada1989). If these amino acids are truly exogenousin origin, they wouldappear to be materialthat some- howsurvived the K/Timpact, were synthesized from meteoritic organics in the post-impactfireball (Oberbeck& Aggarwa11992), or were delivered to Earth interplanetary dust evolvedoff the K/Timpactor (Zahnle & Grinspoon 1990). Anyof these mechanismswould be relevant to early Earth. Furtherexploration of the aminoacid profiles of other K/Tboundary sites is essential for evalu- ating possibleexplanations for the origin of these apparentlyextraterrestrial aminoacids. (The Zhao& Badaresults are for only one site, StevnsKlint, Denmark.)

Photo-Oxidation2+ of Aqueous Fe A possible nonatmosphericmechanism by whichultraviolet photolysis could haveacted as an energysource for prebiotic organicchemistry is the photo- by Stanford University Libraries on 04/23/05. For personal use only. oxidation of aqueohsFe 2+ to generateelectrons and/or H2and thus provide reducing power. H2can be generated from near-UVirradiation of aqueous ferrous hydroxideat pH6-8 (Borowska& Mauzerall 1987), and the presence

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org of bandediron formationsin Archeanrocks has beencited as evidencethat Fe photo-oxidationoccurred on the early Earth (Bratermanet al 1983,Braterman & Cairns-Smith1987). The coupling of Fe photo-oxidationto organic synthetic reactions and protometabolismhas been postulated (de Duve1991) but not shownexperi- mentally.~+ Formaldehydeformation by UVirradiation of aqueousCO2/Fe solutions has beenreported (see Chang1993 for a review),although the synthesis of HCNor carboxylicacids by couplingto Fe photo-oxidationhas not been reported. Evenif this phenomenonoccurs in an ocean, it wouldbe limited to the photic zone. Hartman(1975, 1992) has suggesteda schemefor fixation of inorganiccarbon and nitrogenby ferrocyanidephoto-oxidation in Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 233

conjunctionwith self-replicating clay mineralsystems, but this systemhas not beeninvestigated experimentally.

Hydrothermal Systems Submarinehydrothermal vents (Corliss et al 1979,Von Damm et al 1985)have beensuggested as sites for the originof life on the early Earth(Corliss et al 1981, Baross& Hoffman 1985). Attractive features of vent environmentsfor prebiotic activity includeenergy from thermal gradients, the presenceof chemicalreduc- ing powerin the formof minerals,and possibleprotection from the effects of large bolide impacts(Maher & Stevenson 1988, Sleepet al 1989, Holm1992). It has beenproposed that aminoacids and other organic moleculescould be synthesizedin vent systems(Shock 1990a), and that condensationreactions formamide and ester bonds(such as thosein proteinsand lipids) couldalso take place in vent waters (Ferris 1992, Shock1993). Thesesuggestions are based on the concept that the approachto equilibriumamong C-, H-, O-, and N- containingcompounds is kinetically inhibited underhydrothermal conditions, whichprevents the systemfrom reaching true thermodynamicequilibrium and allowsorganic species to exist in metastableequilibrium states (Shock1990a). Thecalculated equilibrium constants K of reactionsresulting in polymerization of aminoacids to peptides,however, all havevalues ofK < 1 in suchmetastable equilibriumsystems, indicating that the equilibria lie in the directionof the free aminoacids rather than polypeptides(Shock 1992b, 1993). The metastable equilibriumactivities of mostprebiotically relevant species predicted by these studies are 10-5 or less (Shock1990a, 1992a), indicating steady-stateconcen- trations of questionablevalue for further organicsynthesis. Someevidence for a possiblehydrothermal contribution to prebiotic organic chemistrydoes exist in the synthesisof long-chaincarboxylic acids. Schulte& Shock(1993) have calculated equilibrium constants of 104-105for the oxidation

by Stanford University Libraries on 04/23/05. For personal use only. of aldehydesto acids, includingsix- andeight-carbon acids, underhydrothermal conditions,and Shock(1990a) has calculatedactivities of organicacids as high as 10-2 in vent systems. Theproduction of carboxylicacids in this manner would,of course, be dependenton the supply of aldehydesto hydrothermal Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org systems fromexternal sources such as the atmosphere.The possibility of Fischer-Tropschsynthesis of moleculessuch as long-chaincarboxylic acids from COand H2in vent environmentsremains controversial (Miller &Bada 1988,Ferris 1992). Attemptsto test predictions of hydrothermalorganic synthesis experimentally havebeen hampered by the lack of accessto natural submarinevents and the technicaldifficulties involvedin laboratorysimulation of hydrothermalsystems. Thedata of Miller &Bada (1988) are somewhatdifficult to interpret becauseabsolute concentrations are not reported,but they suggestthat the stability of aminoacids other than glycineis lowin vent waterswith temperatures Annual Reviews www.annualreviews.org/aronline

234 CHYBA& McDONALD

of 250°Cor more[but see Shock(1990a,b) for critiques of these experiments]. Hennetet al (1992) reported the synthesis of glycine and small amountsof a few other amino acids in an experimental mineral-buffered hydrothermal system. These experiments were carded out with HCN,H2CO, and ammonia(NH3) starting materials. However,there mayhave been sources of these molecules available on the early Earth, e.g. the photochemical production of ammonia (Summers& Chang1993) and perhaps atmosphere or exogenous sources. Be- cause the maximumduration of these experiments was 54 h, the stability of amino acids over longer times in such a system remains to be explored. Mar- shall (1994) has reported synthesis of amino acids from NH4HCO3,CaC2, Ca, and H202in aqueoussolution at 200-275°(2. The possibility of biogenic amino acid contamination in these experiments cannot be excluded, unfortunately, because the analysis technique used was not capable of full chiral aminoacid resolution and adequate control experimentswere not carried out.

Exergonic Mineral Formation Wachtershauser (1988a,b; 1990a,b) has proposed that synthesis of organic moleculeson the early Earth could have occurred by reduction of aqueous dis- solved CO2to organic compoundson pyrite mineral surfaces. The energy for these reductions wouldbe provided by the exergonicformation of pyrite (FeS2) from FeS and H2S. The negatively charged organic acids produced would be electrostatically held on the positively chargedpyrite mineral surface, wherea surface protometabolismwould develop. Organic molecules would exist in solution only at extremely low concentrations; once they diffused awayfrom the surface they wouldnot return and thus wouldplay no part in further reactions on the pyrite surface. The mechanismsof the initial reduction of CO2to organic compounds,especially the mechanismsof carbon-carbonbond formation, are not clearly de-

by Stanford University Libraries on 04/23/05. For personal use only. fined in this hypothesis (see de Duve& Miller 1991). The equilibrium between water-soluble organic moleculesbound to the mineral surface and the enormous volumeof an essentially organic-free oceanshould lie in favor of desorptionand solution of the organics, althoughthis maybe less of a problemfor hydrothermal Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org interstitial waters in contact with mineral surfaces. Theequilibrium between ad- sorbed moleculeson a surface and moleculesin the surroundingsolution should result in a decrease in surface density of adsorbedmolecules as the solution concentration of the molecules decreases (Lahav & Chang1976). The elec- trostatic binding of organic acids to the pyrite surface must be strong enough to retain the moleculeson the surface, while still allowing the moleculesto migrate along the surface and interact freely with each other in a protometabo- lism. That this is in fact the case in such systemshas not been demonstrated. The formation of FeS2 from FeS and H2S has been shownto generate H2 under laboratory conditions (Drobner et al 1990). Blochl et al (1992) Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 235

reported the reduction of carbon-carbonand carbon-oxygenbonds (alkynes and aldehydes to alkenes and alkanes) in such a system, and Kaschkeet al (1994) have reduced cyclohexanoneto a variety of dithiols in nonaqueoussolvents by this method. However,the central claim of the hypothesis, the fixation of inorganic carbon to organic carbon by FeS2 formation, has not yet been demonstrated experimentally.

Internal Radioisotope Decay Radionuclidedecay would contribute an amountof energy to a planetary crust comparableto electric discharges (Or6 et al 1990), but in a differentiated body the crust wouldprobably be relatively free of reactive organics. Internal radio- genic heating may, however,be important for the synthesis of aminoacids on small bodies such as asteroids throughthe generationof liquid water (Peltzer et al 1984). The decay of 222Rn,a short-lived daughter product of 238U,has been suggested as an energysource for prebiotic chemistryin groundwaters(Martell 1992). One- and two-carbon organic acids have been producedin the laboratory by the self-irradiation of 14C-containingCaCO3 (Albarran et al 1987), and ionizing radiation can convert these moleculesto longer-chain acids in aqueous solution (Negron-Mendoza& Ponnamperuma1982).

Remaining Problems The relevance of laboratory yields from prebiotic experiments to the actual origin of life in a planetary environmentis difficult to assess becausethe mini- mumaqueous concentration of simple organics necessary for the synthesis of biomacromoleculeshas not been firmly established. Most prebiotic chemists wouldprobably agree that, in the absenceof surface catalysts or other concen- by Stanford University Libraries on 04/23/05. For personal use only. tration mechanisms,millimolar steady-state concentrations of simple organics (nitriles, aldehydes,etc) in a prebiotic oceanwould probably be sufficient for the synthesis of biomonomerssuch as amino acids, whereas concentrations

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org below one micromolarwould probably be insufficient. It is possible that surface catalysts such as clays or other mineral surfaces (Cairns-Smith1982; Ferris & Ertem1992, 1993), or vesicles formedabiotically from nonpolar molecules (Morowitzet al 1988), could function as concentrat- ing agents for prebiotic organics and thus lower somewhatthe bulk oceanic concentrations necessary for the origin of life. Until our knowledgeof the oxidation state of the early Earth’s environmentis better constrainedby available geological and geochemicaldata, however, prebiotic chemists will be left to wanderthrough a mazeof possible prebiotic chemicalenvironments and energy sources while the relative importanceof each to the actual origin of life on Earth remains unclear. Annual Reviews www.annualreviews.org/aronline

236 CHYBA& McDONALD THE RNA WORLD The Chicken-and-Egg Paradox In modernbiochemistry, there is a clear division of the two fundamentalfunc- tions necessaryfor life: cod!rig of genetic informationand catalysis of chemical reactions. The former is the exclusive domainof the nucleic acids DNAand RNA,while the latter is performedalmost exclusively by proteins. This clear division of labor in the contemporarycell historically led to a chicken-and-egg paradoxregarding the origin of life: Whichbiomolecules, proteins or nucleic acids, camefirst? Andhow did the earliest organismsperform both the genetic and catalytic functions with either nucleic acids or proteins alone (Dyson1985, Orgel 1986a)? The discovery in the early 1980s by T Cech, S Altmanand colleagues that certain RNAsequences could exhibit limited catalytic activity resulted in (in addition to the 1989 Nobel Prize in Chemistry) the emergenceof a possible solution to the nucleic acid vs protein problemin the origin and early evolution of life. The "RNAworld" (Gilbert 1986) was conceived as an early stage of evolution in which RNAfunctioned as both genetic material and catalyst, without the aid of protein enzymes as we knowthem today. The subsequent characterization of the catalytic abilities of self-splicing ribosomalRNA introns (Zaug & Ceeh 1986, Cech 1990), the RNAsubunit of RNase P (Altman et 1989), and ribosomal RNA(Noller et al 1992) have shownthat RNAfunctions catalytically in significant areas of contemporarybiochemistry. The directed expansionof these catalytic abilities through test-tube evolution (Beaudry Joyce 1992, Lehman& Joyce 1993) and the amplification of inherent catalytic ability in pools of randomRNA sequences (Bartel & Szostak 1993, Prudent et al 1994) have led to a consensusthat RNAis capable of enoughcatalytic diversity and powerto have served as the enzymaticworkhorse of a primitive metabolism. by Stanford University Libraries on 04/23/05. For personal use only.

Lost in the Sugar Forest Whenattention turns to the plausibility of the prebiotic synthesis and survival Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org of RNA,however, problems emerge. RNAis composed of three chemical moieties: the four bases adenine, guanine, cytosine, and uracil (Figure 1), the sequence of which makesup the genetic information; the sugar ribose that forms the backbone of the molecule; and the phosphate group, which links each base-ribose unit to its neighbor. If RNAis to be accepted as a plausible prebiotic molecule, all three of these componentsmust be readily synthesized under reasonable early Earth conditions. Once these building blocks have been made, they must then be joined into base-sugar-phosphateunits knownas nucleotides (Figure 2). The nucleotides must then be polymerized, again under plausible prebiotic conditions, into oligonucleotides long enoughto serve as Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 237

I~H2

HO--P--O--CHa

phosphaS O ~~=~"~-~ sugar

HO OH

Nucleotide (adenosine monophosphate)

O=P~O"

O" O" O"

Orthophosphate Condensedphosphate (pyrophosphate) Figure2 Structureof a typicalribonucleotide, with components indicated, and the structuresof orthophosphateand a condensedphosphate by Stanford University Libraries on 04/23/05. For personal use only.

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org both catalysts and informationcarriers. Finally, these oligonucleotidesmust be capable of catalyzing self-replication through the template-directed formation of complementarystrands. The difficulties faced by these processes in the prebiotic environmenthave been discussed in detail elsewhere (Shapiro 1988, Joyce 1989, Joyce & Orgel 1993, Schwartz& de Graaf 1993); they are briefly summarizedhere. The prebiotic syntheses of the purine and pyrimidine bases of RNAare the least problematic. The demonstration of adenine synthesis by aqueous polymerization of HCNwas one of the early contributions to experimental origin-of-life research (Or6 1960; Or6 and Kimball 1961; Voet & Schwartz 1983). Pyrimidinebases have also been synthesized under plausible prebiotic Annual Reviews www.annualreviews.org/aronline

238 CHYBA& McDONALD

conditions (Sanchez & Orgel 1970). These experiments (reviewed in Ferris & Hagan1984) share the problemof low to moderateyields (typically a few percent) commonto prebiotic synthesis experiments. In addition, these experiments were done by heating dry samples. Dry heating scenarios maynot be relevant to an ocean-coveredArchean Earth, whichlacked large areas of exposed land to contain isolated bodies of water that could undergo evaporation and dry heating. Volcanic island arcs mayhave provided such exposed land in the absence of continental crust, however. Both purines and pyrimidines have been reported in extracts of the Murchisoncarbonaceous chondrite (see Cronin et al 1988). Impactdelivery to the prebiotic Earth is therefore a possible source of nucleic acid bases, although the survival of such organics in large impacts seemsunlikely (Chybaet al 1990). The synthesis of ribose, the five-carbon sugar that forms the backboneof RNA,is even more problematic in the prebiotic environment. The most widely knowngeochemically plausible methodof synthesizing sugars is the formose reaction, which involves the alkali-catalyzed polymerization of an aqueous formaldehydesolution to produce a wide variety of sugars (for a review see Shapiro 1988). Ribose, however, is only a minor componentof the product mixture, and both D- and L-enantiomers of ribose are synthesized in equal amounts(the implications of this racemic mixture are discussed below). The ribose peak in a gas chromatogramlies amidst the manyother products of the formosereaction (Shapiro 1988): It becomeslost in the sugar forest. The concentration of formaldehydeneeded for ribose synthesis (>0.1 M) higher than that likely to have been available in the oceansof the early Earth, and the high pH(> 8) of the alkali-catalyzed reaction maybe higher than that a prebiotic ocean in equilibrium with a CO2-containingatmosphere (Grotzinger & Kasting 1993). Somecommon minerals such as clays have been found to catalyze the formose reaction at neutral pH(Schwartz & de Graaf 1993), but

by Stanford University Libraries on 04/23/05. For personal use only. the other difficulties remain. Furthermore,ribose is prone to decompositionon time scales of at most a few years in the geochemicalenvironment (Larralde Miller 1994). Amore selective synthesis of ribose has been reported by Mulleret al (1990).

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org This involves the preferential formationof ribose diphosphatefrom glycolalde- hyde phosphate in an aqueous NaOHsolution (again with a pHprobably higher than that of the prebiotic ocean). The suggestedprebiotic precursors to glyco- laldehyde phosphateare aziridine carbonitrile and oxirane carbonitrile (Wagner et al 1990, Eschenmoser1993). Althoughthese molecules mayexist in the in- terstellar medium,their stability in a planetary environmentis open to question and the ribose diphosphateproduced in this reaction is also racemic. Inorganic phosphate was no doubt present on the early Earth. The concentration in the ocean, however,would have been limited by solubility to approx- imately the current oceanic value of 0.07 ppm(Pinet 1992). Moreimportantly, Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 239

this wouldhave been almost exclusively orthophosphate, PO~-3, with no high- energybonds available to drive further reactions. To participate in the polymerization of nucleotides to oligonucleotides, phosphate must be in the form of condensed phosphates (phosphates containing high-energy phosphodiester bonds) such as meta- and polyphosphates (Figure 2). Pyrophosphatecan con- dense from orthophosphate in aqueous solution in the absence of condensing agents, with yields of up to 50%at 160°C(Rabinowitz et al 1968) but <0.1% at 37°C (Hermes-Lima1990). With thioesters added as condensing agents, yields of several percent based on orthophosphate can be obtained (Weber 1981, 1982), but the availability of prebiotic thioesters is unclear. Urea can also function as a phosphatecondensation catalyst, but only at temperatures around 100°C(Osterberg & Orgel 1972). The high temperatures and the acidic form of orthophosphateneeded for these reactions maycast doubt on their plausibility in an early Earth environment,although someearly Earth modelsimply very dense COzatmospheres with surface temperatures of 85-110°C(Kasting & Ackerman1986). Laboratory simulations and analyses of collected volcanic gases indicate that somepolyphosphates can be producedby partial hydrolysis of P40~0in magma(Yamagata et al 1991).

Putting the Pieces Together Even if we assume that the three major componentsof RNA--bases, ribose, and condensedphosphates--were available on the prebiotic Earth, there are more hurdles to leap to make RNA.RNA is a polymer composedof monomer nucleotide units, whichconsist of one base, one ribose molecule,and one phosphate anion. Nucleosides (nucleotides minus the phosphate) have been producedby heating dry mixtures of bases and ribose (Fuller et al 1972) as well from ribose, cyanamide,and cyanoacetylenein the presence of UVirradiation (Sanchez & Orgel 1970). Muchof the product yield in these experiments, how- by Stanford University Libraries on 04/23/05. For personal use only. ever, wasin the formof nonbiologicalisomers of the nucleotides, and the prebiotic plausibility of dry heating in the presenceof a possible global oceanis open to question. Adenosine(adenine nucleoside) has also been reported as a product

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org of UVirradiation of adenine/ribose solutions (Ponnamperumaet al 1963). Nucleotide synthesis from nucleosides and inorganic phosphate under possible prebiotic conditions has been achieved to somedegree. Lohrmann& Orgel (1971) generatednucleotides, including 2P-3r cyclic nucleotides, by dry heating a mixture of nucleosides, urea, and inorganic phosphate on hydroxylapatite at 65-100°C. Lohrmann(1975) reported synthesis of nucleoside polyphosphates from dry heating of nucleoside monophosphatesand trimetaphosphate. Cyclic nucleotides and nucleoside polyphosphatesare particularly important because they contain high-energy phosphate bonds and can polymerize into oligonucleotides without additional condensingagents (Verlander et al 1973). Catalysis of nucleotide polymerizationreactions by clay minerals has also been Annual Reviews www.annualreviews.org/aronline

240 CHYBA& McDONALD

investigated (Ferris 1993; Ferris & Ertem 1992, 1993) and mayhave played role in oligonucleotide formation on the early Earth, but the requirementfor activated nucleotides is not eliminatedby the use of clays. The final and most important step on the road to the RNAworld is the use of spontaneouslypolymerized oligonucleotides as templates, in the absence of protein enzymes,to achieve replication and information transfer, i.e. to serve as a genetic material. Here, more serious problemsemerge. The efficiency of nonenzymatictemplate-directed oligonucleotide synthesis is heavily dependent on the base sequenceof the nucleic acid used as the template (see Orgel 1986a, b). The complementarystrand to the template can be synthesized with relative ease in these experiments, but the subsequentuse of that complementarystrand to synthesizea copyo.f the original templateis severelyrestricted. This problem can be overcomeat least in simple laboratory systems, as shownby recent work using double-stranded DNAcomplexes as templates for self-replication (Li Nicolaou 1994) and other work demonstrating self-replication in a system of self-complementary and cross-complementaryo!igonucleotides (Sievers &von Kiedrowski 1994). In addition, the experiments done so far (e.g. Joyce et al 1984, Acevedo Orgel 1986) have used nucleotides activated with imidazole or included condensing agents such as carbodiimides, moleculesthat maynot have been readily available on the early Earth (howeversee Ferris & Hagan1984). Perhaps most critical is the observationthat the use of a mixtureof D- and L-ribonucleotides in template-directed polymerizationexperiments results in a severe inhibition of oligonucleotide synthesis (J0yce et al 1984). Since no unambiguouscom- pelling mechanismfor the abiotic origin of chirality has been demonstrated (Bonner1991), and since no prebiotic synthesis of ribose or any other sugar nknownto result in an excess of one enant!ome,rover the other, chiral inhibitio of nonenzymaticRNA formation maybe the single most daunting obstacle to

by Stanford University Libraries on 04/23/05. For personal use only. e.the use of RNAas the first biomacromolecul

Alternatives to RNA

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org The problemswith the prebiotic synthesis and stability of RNAare well known in the origin-of-life community,and several possible alternatives to the modern RNAstructure have been proposed and investigated. The most conservative of these involve structural isomers of RNAin which the bases are linked to the ribose at different positions in the base ring structure from those in modern nucleic acids. As mentioned above, it has been observed (Sanchez Orgel 1970, Fuller et al 1972, Maurel & Convert 1990) that synthesis of nucleosides from bases and ribose under prebiotic conditions results in higher yields of structural isomerssuch as Nr-ribosyladenine, and somecatalytic activity has been reported in these isomers (Maure! & Decout1992). Nucleoside analogs containing modified bases such as 8-hydroxymethyladenineor urazole Annual Reviews www.annualreviews.org/aronline

ORIGINOF LIFE 241

(Schwartz & Bakker 1989, Robertson et al 1994, Kolb et al 1994) have also been suggestedas possible componentsof the first nucleic acids. Moreradical ideas for nucleic acid analogs involve substitution of another sugar for ribose in the molecular backbone. Three- and four-carbon molecules such as glycerol, acrolein, and erythritol could fill the chemicalrole of ribose in nucleic acid analogs and might have been more easily synthesized on the early Earth (Joyce et al 1987, Joyce 1989). The lack of chiral cen- ters in these moleculeswould also eliminate the problemof chiral inhibition of oligomerization discussed above. Pentaerythritol, a five-carbon reduced sugar, can be synthesized by a photochemically catalyzed formose reaction (Shigemasaet al 1977) and has also been postulated as a prebiotic replacement for ribose (Schwartz 1993, Schwartz & de Graaf 1993). These nucleic acid analogs, however,may be too flexible to formstable double-strandedstructures (SL Miller, personal communication).Nucleic acid analogs based on hexoses such as glucose, allose, and altrose formmore stable double-strandedstructures than does DNA(Eschenmoser 1993), but this property is not necessarily advan- tageous. If nonstandardbase-pairing schemesare as stable as the Watson-Crick base pairs that are the basis of the genetic code, a given base sequence may act as template for the replication of both complementaryand noncomplemen- tary base sequences. The transfer of genetic information would be seriously disrupted in such a case. Perhaps the most intriguing nucleic acid analogs currently under study are peptide nucleic acids (PNAs). These are synthetic molecules consisting the normal nucleic acid bases with a backboneof 2-(aminoethyl)glycine units (Egholmet al 1992a). These molecules form stable double-stranded structures both with each other and with DNA,following normal Watson-Crick base- pairing rules (Egholmet a11992b). The amino acid componentof the backbone is probably a moreplausible prebiotic moleculethan ribose or other sugars,

by Stanford University Libraries on 04/23/05. For personal use only. but the polymerization of bases and amino acids to form PNAshas not been demonstratedin a prebiotic setting. Althoughthe possible role of PNAas the first genetic material has been discussed (Nielsen 1993), the catalytic potential of PNAhas yet to be explored. The suitability of PNAas a substitute for RNA

Annu. Rev. Earth. Planet. Sci. 1995.23:215-249. Downloaded from arjournals.annualreviews.org in the RNA-worldscenario remains unclear.

Future Outlook Joyce & Orgel (1993) conclude that at this point the original chicken-and- egg prol~lemregarding the evolution of catalytic and informational biomacromolecules appears to have been solved, only to be replaced by another. A self-replicating biomacromoleculeas complexas RNAmust, it seems, evolve its catalytic self-replicating activity throughnatural selection; natural selection, on the other hand, requires a self-replicating informational biomacromolecule to serve as the genetic material. Szostak & Ellington (1993), however, point Annual Reviews www.annualreviews.org/aronline

242 CHYBA& McDONALD

out that RNApopulations with randomsequences can contain someindividual RNAsequences that are able to bind organic molecules, and so it maynot be unreasonableto expectsome catalytic self-replicating activity to arise in the absenceof Darwinianevolution. Therecent in vitro workin RNAevolution discussed aboveindicates that, given a mechanismfor evolution, RNAcan acquire a wide range of catalytic specificities andcan possiblybe as efficient a catalyst as protein(Cech 1993). Giventhe problemswith prebiotic RNAformation discussed above, it seemsthat the plausibility of an early biochemicalsystem dependent entirely on nucleic acids rests on the demonstrationof catalytic activity in a nucleic acid analog moreprebiotically plausible than RNA.

ACKNOWLEDGMENTS Theauthors wish to thankJeffrey Bada,James Ferris, GeraldJoyce, Christopher McKay,and Carl Saganfor commentson various portions of this manuscript. GDMwas supported by a fellowship from the NASASpecialized Center of Researchand Training (NSCORT) in Exobiologyat the University of California, San Diego.

AnyAnnual Review chapter, as well as anyarticle cited In an AnnualReview chapter, maybe purchasedfrom the AnnualReviews Preprints and Reprintsservice. 1-800-347-800"/;415-259-5017; email: [email protected]

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