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    Thinking ofBiology

    Asteroid impacts, microbes, and the cooling of

    the atmosphereE arth 's surface temperatureconstrained microbial evolu-tion, according to Schwartz-man et al. (1993). Their hypothesisstates that the maximal temperaturethat extant organisms of a giventype tolerate is the surface temp era-ture occurring when that type oforganism arose. Schwartzman andhis colleagues concluded that thetemperature changed from 100C to

    50C between 3.75 billion y ears ago(BYA) and 1 BYA. These tempera-tures are consistent with those de-rived from oxygen isotope ratios inanc ien t sed iments (Karhu andEpstein 1986, Knauth and Lowe1978). The 100C surface tempera-ture they derive for 3.75BYA is alsothe same as E arth's surface temp era-ture 4.4 BYA (Kosting a nd Acker-man 1986).

    In this artic le,we address the causeof the delay in surface cooling until3.75 BYA, and we explore the impli-cations for microbial evolution of ahigh temperature on early Earth.We propose that three effects of theearly heavy bombardment of Earthby asteroids and comets, until 3.8BYA, could have delayed onset ofsurface cooling.

    In the beginning . . .Soon after Earth accreted 4.4 BYA,there was a global ocean, and Earth'satmosphere had as much as 20 at-mospheres of carbon dioxide, whichcaused a high level of greenhouseheating. Temperatures could nothave declined un til the carbon diox-ide was removed through weather-ing of continental rocks, which lib-crated metal ions that combined withcarbonic acid to form carbonaterocks.

    by Verne R. Oberbeck andRocco L. MancinelH

    A considerable period of time mayhave been required to form the firstcontinents. Planetesimals, asteroids,and comets that hit Earth's surfaceduring the first 700 million years ofits history could have created thefirst land masses. However, impactbasins formed during the early heavybombardment would also have vola-tilized any carbonate rocks that hadformed as a result of weathering of

    continents; this volatilization wouldhave released carbon dioxide backto the atmosphere and would haveprolonged the initial high levels ofgreenhouse heating even in the pres-ence of continents.

    Finally, until 3.8 BYA, large im-pact events could have preventedthe habitation of land masses bymicrobes that would, according toSchwartzman and Volk (1989) andSchwartzman et al. (1993), havebeen able to accelerate chemical

    weathering of continental rocks, re-moval of carbon dioxide from theatmosphere, and cooling. We pro-pose that the sequence of microhialevolution consistent with the earlyheavy bom bardm ent and a high tem-perature of early E arth is: hetero tro-phs, chemoautotrophs, and finallyphotoautotrophs.

    The case for a hightemperature on early E arth

    Earth's surface temperatures, de-rived from the biota (Schwartzmanet al. 1993), are actually com patiblewith temperature estimates that hadbeen derived previously from oxy-gen isotope ratios oi sediments(Knauth and Epstein 1976). Never-theless, Perry et al. (1978) rejectedthe high-temperature interpretationof isotopic data for early Earth be-cause they interpreted the Precam-brian tillites to be glacial deposits.Theoretical climatic models indi-

    cated that, if glaciation occurred,

    the maximal Precambrian tempera-ture must have been on the order ofIQ^C (Kasting and Toon 1989).However, because an as-yet-un-known fraction of Earth's ancienttillites and diamictites (clastic de-posits resembling glacial tills) aredeposits of impact craters rather thandeposits of glaciers (Marshall andObe rbeck 1 992, Oberb eck andAggarwal 1992a, Oberbeck andMarshall 1992, Oberbeck et al .1993, Rampino 1992, Sears and Alt1992), the existence of early glacia-tions and a 2O''C upper temperaturelimit for the Precambrian climatehas been questioned (Schwartzmanetal . 1993).

    Perry et al. (1978) proposed thatthe variation in oxygen isotope ra-tios in sediments was due to thetemp oral ch ange in "*O in seaw ater,or alteration of sediments duringburial in a closed system and notclimatic variation. However, K nauthand Lowe (1978) published a studyof Precambrian cherts, includingthose formed at the sediment/waterinterface, that appears to excludethe possibility of diagenesis. Thetemperature history of cherts be-tween 3.5 BYA and the pre sent isquite similar to that which has nowbeen inferred from the evolution ofthe biota by Schwartzman et al.(1993) . F ina l ly, Holmden andMuehlenbach (1993) concluded,

    from the study of oxygen isotopeprofiles of two-bill ion-year-oldophiolite mineral deposits, that thelow oxygen isotope ratios of Prot-erozoic rocks and cherts do not re-flect temporal depletions of '"O inseawater. Thus, we adopt the viewthat oxygen isotopic data suggest ahigh-temperature Precambrian cli-mate.

    Additional arguments have beengiven against early glaciation andthus for a high-temperature earlyEarth. Schermerhorn (1974) chal-

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    lenged the prevailing view that Pre-cambrian tillites atid diamictites,especially those that occur alongancient continental breakup mar-gins, are of glacial origin. He identi-fied the textural criteria that had,until 1974, heen used to identifytillites and diamictites as glacialdeposits, and he argued that thedeposits could have been producedby tectonism. Additionally, Salop(1983) pointed out that sedimentsbounding many ofthe ancient tillitesand diamictites are those formed inwarm-water environments. He pos-tulated that the abrupt low-tempera-ture excursions at the tilUte anddiamictite horizons can only be ex-plained by glaciations if glaciationsoccurred suddenly in the midst of ahot climate. Knauth and Lowe(1978) also suggested that glacial

    periods do not preclude hot inter-glacial periods.

    The ideas o f Schermerhorn(1974), Salop (1983), and Oberbecket al . (Oberbeck and Aggarwal1992a,b, Oberbeck and Marshall1992, 1993) strengthen the long-standing, and previously largely ig-nored, isotopic evidence for a hightemperature of early Earth (Knauthand Lowe 1978). To this evidencewe can now add the inferences ofSch wartz ma netal. (1993). It is note-worthy that the temperature curvesderived by them are quite similar tothose for the same time periods de-rived from isotope data by Knauthand Lowe (1978).

    Schwa r tzm an et a l . (199 3)pointed out that their temperaturehistory (Figure 1; between 3.75 and2.5 BYA) was consistent with isoto-pic data but higher than other esti-mates based on equilibrium condi-tions for mineral precipitation. Forexample. Walker (1982) cited pri-mary evaporite gypsum precipita-tion in 3.5 billion -year -old sedi-ments to determine the uppertemperature limit of 58C for sur-face-water temperature rather than73C (Figure 1), which would be theupper limit if the sediments wereprecipitated in freshwater. The limitwould he even lower if gypsum wasprecipitated in seawater. However,Schwartzman et al. (1993) arguedthat m etastable precipitation of gyp-sum is likely at temperatures farabove its stability field and would

    Time (billions yrs ago)

    Figure 1. Surface temperature historyof Earth. Temperatures after 3.75 BYAare from Schwartzman et al. (1993),and those hefore 3.7,S BYA are inter-preted in the text.

    be consistent with a surface tem-perature of 73C at 3.5 BYA.

    Because the isotopic data ofKnauth and Lowe (1978) give thesame temperature change with geo-logic history as those of Schwartz-man et al, (1993), because it is be-coming increasingly difficult toexplain the oxygen isotope data bytemporal changes in isotopic com-position of seawater or diagenesis,and because Knauth and Lowe(1978) interpret the changes in iso-topic ratios to reflect climatic varia-tions, we ado pt the surface tempe ra-ture change shown in Figure 1. A

    key feature of this curve, for thisstudy, is the lOCC temperature at3.75 BYA that declines to 73C by3.5 BYA and defines the onset of cool-ing of the near-surface environment.

    The onset of cooling of theatmosphereWe now consider the cause of thedelay in cooling of the atmosphereuntil 3.75 BYA and the im plication sof this delay for microbial evolu-tion. Earth's atmosphere during itsfirst few hundred million years, iustafter condensation of the oceans,may have contained up to 20 bars ofcarbon dioxide. Kasting and Acker-man (1986) modeled the dependenceof surface temperature of Earth'searly atmosphere on such an atmo-spheric carbon dioxide partial pres-sure, and they concluded that thetemperature was in the range of85-110C. !n Figure 1, we combinethe inferred surface temperaturesafter 3.75 BYA (Schwartzman et al.

    1993) with a temperature of 1at 4.4 BYA. The temperature hisuggests that from approxim4.4 BYA to 3.75 BYA the sutemperature was constant atproximately 100*C. This proloconstan t surface temp erature haportant implications for coolinatmospheres of bombarded pl

    and for microbial evolution.We propose that the cause o

    delay in the onset of cooling the prob able 100C surface temture at 4.4 BYA until 3.75 BYAdue to three effects ofthe early hbombardment of Earth that launtil approximately 3.8 BYA. Fsome period of time was requirform the continents so that cnental rocks could have been aable for chemical weatheringassociated cooling from remov

    carbon dioxide from the atmospLarge-impact cratering eventscurring during the early heavy bardm ent, would have required time to produce the first top ogr adichotomy of continents and obasins (Frey 1980) so that weaing and cooling could occur. ond, the heavy bombardment would have caused release ofbon dioxide back to the atmospby impact volatilization of caate rocks and thus sustained

    high level of initial greenhouse ing until 3.8 BYA. Finally, the hbombardment could also have odically sterilized Earth and decontinuous habitation of microrganisms on land masses andvented acceleration of chemweathering of silicate rocks ansociated cooling until the end obombardment .

    Consider the formation ofoceans and the time needed to the silicate rocks of the continChyba (1987) calculated thacomets contained 10% water, during the early bom bardm ent ets supplied enough water to to account for the current ovolume. Frey (1980) argued thearly as 4.4 BYA, Earth was dentiated into a sialic igneous crust with a higher-density mand a glohal ocean. In his large asteroid impacts had, byBYA, produced the topographichotomy of continents and oc

    Isotopic data also suggest that

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    tinents first existed at some timebetween 4.3 and 4.0 BYA (Bowringet al . 1 989). The initial global ocean ,a product of comet impacts, wouldhave prohibited removal of atmo-spheric carbon dioxide because rockswere not exposed to weathering.However, if land masses were inplace after 4.0 BYA, cooling of the

    atmosphere by removal of carbondioxide through weathering of sur-face silicate rocks could, in the ab-sence of other adverse factors, havebeen started at this time.

    One such adverse factor is impactvolitalization of carbonate rocks,which would have recycled carbondioxide to the atmosphere andhelped to sustain the high initialsurface temperatures on Ear ththrough greenhou se heating until theend of the heavy bombardment. This

    mechanism might have kept enoughcarbon dioxide in the atmosphere ofMars until the end of the heavybombardment of the inner planetsat 3.8 BYA, so that surface tem pera-tures remained above freezing, liq-uid water existed, and surface run-off channels formed (Carr 1989).Sti l l another impact mechanismcould have retarded cooling until3.8 BYA.

    Microbial enhancement of conti-nental rock weathering would have

    facilitated surface cooling (Schwartz-man and Volk 1989} if microbes werepresent on continents at 4.0 BYA un-der the suggested habitable temper-ature conditions (Figure 1). Howev-er, another adverse effect of impactsmay have delayed the weath ering ofcontinental rocks in place by 4.0BYA. Recent developments in thefield of impact catastrophism indi-cates that microbial life may nothave existed continuously or for sig-nificant periods of time on conti-nental land masses until 3.8 BYA.Maher and Stevenson (1988) ad-vanced the notion that impacts oflarge planetesimals, asteroids, andcomets during the heavy period ofbombardment of Earth, until 3.8BYA, could have period ically steril-ized Harth, frustrated the origin oflife, or killed any existing organisms.

    Sleep etal. (1989) calculated thatthe last impacts that completely va-porized the ocean could have oc-curred as early as 4.4 BYA and aslate as 3.8 BYA. O ber bec k and

    Fogleman (1989b, 1990) found thatthe last ocean-vaporizing impactcould have occurred at 3.8 BYA.Therefore, life may not have beencontinuously present, even in thedeep o cea ns, un til after 3.8 BYA. Ifso, the lack of continuous life onEarth's land surfaces until after 3.8BYA, due to the heavy bombard-

    ment, may be another cause for thedelay in onset of cooling of the near-surface environment.

    He te ro t roph ic and chemoau-totrophic organisms could have ex-isted continuously in the deep oceansafter 3.8 BYA, because there wouldthen have been no ocean-vaporizingimpacts that killed deep sea life butonly ones that sterilized the surface.Therefore, microbes could have con-tinuously evolved and colonized theland surfaces after 3.8 BYA from

    these continuously available stocks.The sustained decline in Earth 's sur-face temperature may have beendelayed until 3.75 BYA (Figure 1) ifocean-vaporizing impacts occurreduntil the end of the bo m bardm ent, ifintermittent but extensive land eco-systems were created only after 3.8BYA, and if these microbial ecosys-tems were effective in acceleratingremoval of carbon dioxide from theatmosphere.

    All of the impact mechanisms for

    delay in cooling seem consistent withthe o nset of coolin g a t 3.75 BYA asinferred here from the isotopic data(Knauth and Lowe 1978), inf^erencesfrom biology (Schwartzman et al.1993), and the probable tempera-ture 4.4 BYA (Kasting and Ackerman1986). Impacts initially produced aglobal ocean that prohibited rockweathering and cooling; they couldalso have been responsible for a va-riety of other processes that kept the10-20 bars of carbon dioxide presentin the atmos phere u ntil 3.8 BYA.Then , 50 m illion years later, coolingbegan when continents existed, noocean-vaporizing impacts occurred,continental microbial ecosystemswere possible, and there was mini-mal impact recycling of carbon di-oxide.

    Implications formicrobial evolutionIf the earth's temperature was con-

    stan t at 100C until 3.75 BYA and

    then cooled rapidly to 73''C by 3.5BYA, and if con tine nta l mic robesaccelerated this cooling of the sur-face (Schwartzman et al. 1993), or-ganisms must have occupied the sur-face of continental land mass soonafter the impact bo mb ardm ent ended3.8 BYA. The imp lication is tha t thesurface organisms evolved rapidly

    from deep-sea organisms that wouldonly have been present continuo uslyafter the last ocean-vaporizing im-pact no later than 3.8 BYA.

    No direct evidence exists for theevo lution of life before 3.8 BYA,leading to controversy over the se-quence of microbial evolution. Wenow link the impact history of earlyEarth (Chyha et al. 1990, Maherand Stevenson 1989 , Ob erbeck andFogleman 1989a,b, 1990, Sleep etal. 1989 ), 16S rRNA phylogenetic

    trees (Woese and Pace 1993), clima-tology (Kast ing and Ackerman1986), and the hypothesis that theupper temperature limit for growthof microbial groups corresponds tothe actual surface temperature ofEarth at the time of the gro up s' firstappearance (Schwartzman et al .1993) to show that each of thesemethodologies independently sug-gests the same sequence of micro-bial evolution on Earth from 4.4 to3.5 BYA. We propose that this se-quence of evolution is: anaerobicheterotrophs, followed by chemo-autotrophs, and finally photoau-tot rophs .

    The early bombardment of Earthbefore 3.8 BYA prev ented life fromgaining a foothold at Earth's sur-face and constrained it to the dark,deep ocean (Maher and Stevenson1988 , Oberbeck and Fogleman1989a,b, 1990, Sleep et al. 1989).On the other hand, the supply oforganic mass from impacting com-ets (Clark 1988, Oro 1961) was alsogreatest during this period (Chybaetal. 1990, Oberbeck and Aggarwal1992b, Oberbeck et al. 1989). Wepropose that comets were the sourceof organic nutrients that sustained asmall biomass of organisms, limitedby the distribution of organics, inthe hot, deep ocean just after theheavy bombardment. Thus, we sug-gest that the earliest microbial formswere thermophilic anaerobic hetero-trophs.

    After 3.8 BYA, the rate of impacts

    March 1994 175

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    decreased and the surface could beinhabited. This development hadtwo effects: it decreased influx oforganic matter, and it allowed thesurface of Earth to become continu-ously inhabited. The limited supplyof organic matter in the presence ofabundant carbon dioxideat the sur-face then gave a selective advantage

    to chemoautotrophs over heterotro-phs. According to the temperatureat which these types of organismsnow live (up to 110C; Kristjanssonand Stetter 1992), this change inadvantage may have occurred atapproximately 3.75 BYA (Figure 1).

    Removal of carbon dioxide fromthe atmosphere through chemoau-totrophy then allowed Farthto coolmore rapidly than by abiotic pro-cesses a lone. We suggest thatchemoautotrophy evolved earliert h an p h o t o a u t o t r o p h y b e ca u sechemoautotrophs can live in deeper,dark regions of the ocean, whichwould have been habitable beforesurface environments, and chemo-autotrophs can tolerate highertem-peratures than photoautotrophs.Thus, impacts together with chemo-autotrop hy may have determinedthetime of onset of cooling of Earth'sa tmosphere at 3.75 BYA. Thenphotoautotrophy evolved.

    Surface-sterilizing impacts ca-pable of vaporizing the photic zoneof the oceans occurred after the lastocean-vaporizing im pact, perhaps aslate as 3.5 BYA (Oberbeck andFogleman 1989a,b, 1990, Sleep etal. 1989). Thus, photoautotrophscould have been intermittentlypresent after 3.8 BYA and continu-ously present at Earth's surface af-ter 5.5 BYA. This presence was alsoimplied by the microbial evolutionscheme put forward by Schwartzmanet al. (1993), in which the tempera-

    ture tolerance of existing organismsreflects Earth's surface temperaturewhen that type of organism firstevolved. The 73''C maximal toler-ance observed in existing photoau-totrophs (Meeks and Castenholz1971) is thus the temperature ofEarth 's surface at 3.5 BYA, just afterthe last surface-sterilizing impact.Itwould not be surprising if modernphotoautotrophs would have thesame upper limit of tolerance totemperature as thecyanobacterialikeorganisms of 3.5 BYA represented

    by the fossil record (Schwartzmanetal . 1993).

    We propose that the sequence ofmicrobial evolution, which is con-sistent with impact constraintsandthe hypothesis that tem perature con-strained microbial evolution (Schwartz-man et al. 1993), is as follows: an-aerobic heterotrophs followed by

    chemoautotrophs (extant examplesinclude Pyrococcus: maximal tem-perature, 1O5''C;and Pyrodictium:maximal te mp erature , 11OC; Krist-jansson and Stetter 1992), with thephotoautotrophs arising later (e.g.,Synechococcus lividus: maximaltemperature, 73C; M eeksand Cas-tenholz 1971).The branching orderdepicted by 16s rRNA phylogenetictrees also suggests that photoauto-trophy arose after heterotrophyandchemoautotrophy (Woeseand Pace1993). We suggest that heterotro-phy arose no later than 3.8 BYA,chemoautotrophy arose approxi-mately 3.75 BYA, and photoauto-trophy arose approximately 3.5BYA.

    The climate history and path ofevolution of the biosphere of anyhabitable planet may be fixed, inpart, by its unique early-impacthis-tory. The decline in surface tem-perature may have been determinedby the impact history of Earth andby microbial evolution.

    Consider the possibilities if theimpact history had been different. Ifthe heavy bombardment of Earthhad been more prolonged,the pla-teau of constant temperature (Fig-ure 1) may have extended in time. Inthat event, the surface temperaturewould not have reached habitablelevels for many types of organismsuntil much later. If so , the evolutionof chemoau totrophy and photoa uto-trophy from the heterotrophs mayhave proceeded later, which could

    have delayed the evolution of morecom plex life forms. The implied syn-ergism between the astrophysicalenvironment and the biospheresug-gests that global change in climateand the biosphere has its roots inastrophysics.

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