Archaea and Eukarya From volcanic origins of chemoautotrophic life to Bacteria

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From volcanic origins of chemoautotrophic life to Bacteria,
Archaea and Eukarya

Günter Wächtershäuser

Phil. Trans. R. Soc. B 2006 361, 1787-1808
doi: 10.1098/rstb.2006.1904
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Phil.Trans.R.Soc.B(2006)361,1787–1808
doi:10.1098/rstb.2006.1904
Publishedonline7September2006
From volcanic origins of chemoautotrophic
life to Bacteria, Archaea and Eukarya
Gu¨nter Wa¨chtersha¨user1,2,*
180333 Munich, Weinstrasse 8,Germany
2209 Mill RaceDrive, Chapel Hill, NC27514,USA
Thetheoryofachemoautotrophicoriginoflifeinavolcaniciron–sulphurworldpostulatesapioneer
organism at sites of reducing volcanic exhalations. The pioneer organism is characterized by a
composite structure with an inorganic substructure and an organic superstructure. Within the
surfaces of the inorganic substructure iron, cobalt, nickel and other transition metal centres with
sulphido,carbonylandotherligandswerecatalyticallyactiveandpromotedthegrowthoftheorganic
superstructurethroughcarbonfixation,drivenbythereducingpotentialofthevolcanicexhalations.
This pioneer metabolism was reproductiveby an autocatalytic feedback mechanism. Some organic
products served as ligands for activating catalytic metal centres whence they arose. The unitary
structure–function relationship of the pioneer organism later gave rise to two major strands of
evolution: cellularization and emergence of the genetic machinery. This early phase of evolution
ended with segregation of the domains Bacteria, Archaea and Eukarya from a rapidly evolving
populationofpre-cells.Thus,lifestartedwithaninitial,direct,deterministicchemicalmechanismof
evolutiongivingrisetoalater,indirect,stochastic,geneticmechanismofevolutionandtheupward
evolutionoflifebyincreaseofcomplexityisgroundedultimatelyinthesyntheticredoxchemistryof
the pioneer organism.
Keywords: iron–sulphur-world; surface metabolism; ancestralgenome; nickel; carbonfixation;
ligandfeedback
1.INTRODUCTION merely combined covalently and sequentially without
Themoleculesofextantlifemaybeclassifiedintofour undergoing redox changes or substantial changes of
categories of different complexity: inorganic nutrients, their electron configurations. The fourth category of
low-molecular organic compounds, polymers and complexityismadeupofparticles:aggregatesofseveral
aggregates of polymers. The first category, the polymer molecules as such or embedded in a lipid
inorganic nutrients of life, consist of molecules of a membrane.
fewatoms,suchasH ,N ,H O,H S,NH ,CH ,CO, For100years,afterthepioneeringworkofvonNa¨geli
2 2 2 2 3 4
CO , HCN and P O . They are gaseous or volatile (1884),mosttheoriesontheoriginoflifehavelocated
2 4 10
andescape from the interior of the Earthas magmatic theemergenceofthefirstreproducingorganismoflifeat
(or volcanic) exhalations. Upon cooling of the flow of orabovethehighlevelofmolecularcomplexityincrease
magmatic exhalations, gaseous H O condenses to frommonomerstomacromolecules.Asaconsequence,
2
liquid water,the elixir of life. theformationofthemonomersisplacedinanobscure
The gaseous nutrients enter the so-called inter- ‘prebiotic broth’, wherein low-molecular compounds
mediarymetabolismoftheextantorganismsandform are believed to have accumulated over thousands or
a few hundred low-molecular bioorganic compounds, millions of years. These theories have been widely
which constitute the second category of molecular reviewed(deDuve1995,2002,2005;MaynardSmith&
Szathmary1995;Zubay1996;Brack1998;Lahav1999;
complexity.Thismaybeseenasthechemicallycreative
Fry2000;Wills&Bada 2000;Hazen 2005;Rauchfuß
part of biochemistry. The gaseous nutrients enter
2005;Thoms2005).Theyareflawedinmultipleways.
syntheticpathwayswithredoxreactionsandthorough-
Here, it should suffice to note that they all postulate
going transformations of the electron configurations.
liquid water and that it is precisely the mass effect of
Some of the low-molecular bioorganic compounds
liquidwater,whichtendstopreventtheaccumulationof
arebifunctionalmonomers(e.g.aminoacids),capable
polycondensation products (or polycondensation
of undergoing polycondensations to high-molecular
agents)duetohydrolysis.
polymers, such as proteins or nucleic acids. This
constitutesthethirdcategoryofmolecularcomplexity.
It is not so much a chemically creative stage as an
2.THE PIONEERORGANISM
organizational stage, in which the monomers are
The failures of the theories of an origin of life by
polycondensation in a ‘prebiotic broth’ posed the
*[email protected] challenge whether it would not be possible to develop
a theory of an origin at the level of low-molecular
Onecontributionof19toaDiscussionMeetingIssue‘Conditionsfor
theemergenceoflifeontheearlyEarth’. organic compounds. As a solution to this problem,
1787 Thisjournalisq2006TheRoyalSociety
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1788 G. Wa¨chtersha¨user Volcanic origin of chemoautotrophic life
that fresh transition metal precipitates (Drobner
CO CO COS NH H S N H HCN
e 2 3 2 2 2
et al. 1990; Huber & Wa¨chtersha¨user 1997,
n
v free volcanic 1998,2003;Huberetal.2003)haveaparticularly
ir diffusion liquid highactivity.
o water (ii) Cody et al. (2000) made the important obser-
n phase vationthatunderhighpressureandtemperature
m.
Fe CO mobilizes FeS to low-molecular carbonyl
o OH organic derivativesofunknownstructure.Thesemaybe
r Ni Fe superstructure transportedthroughvolcanicflowchannelstothe
g Fe Ni S Ni
a S Fe CO Fe siteofthepioneerorganismandbecomeadsorbed
S CO
ni Fe H O Ni S OH mineral ontoorabsorbedintotheinorganicsubstructure.
s H2O S 2 S H2O substructure (iii) Ithasbeenfoundexperimentallythatanumberof
m Ni Fe synthetic reactions are dependent on alkaline
Fe H O OH
2 conditions (Huber & Wa¨chtersha¨user 1998,
2003;Huberetal.2003)andthatthepHofthe
Figure 1. Cross-sectional representation of the minimal
reaction medium may be stabilized by alkaline
organizationofthepioneerorganism.
precipitates, like calcium hydroxide, magnesium
a theory of a chemoautotrophic origin from inorganic hydroxideorbasicmagnesiumcarbonate.There-
starting materials was developed (Wa¨chtersha¨user fore,suchpHbuffersmayalsobeimportantinthe
1988b–d, 1990, 1992). This theory has been dubbed substructure.
‘iron–sulphur-world’ theory for reasons of the geo-
It has been stressed earlier that the inorganic
chemical ubiquity of FeS and the catalytic, energetic
substructure itself undergoes a chemical redox pro-
and structural roles of iron and sulphur at the origin
gressionaccordingtoOstwald’sruleofstepsfromFeS
and during early evolution. I call the first organism of
to FeS . This notion may now be expanded to
life‘pioneerorganism’.Theterm‘organism’standsfor 2
heteroleptic (Fe,Ni)-precipitates progressing through
anorganizedbeingandtheterm‘pioneer’standsforits
carbonylations and sulphidizations. The surfaces of
roleasthestartingpointofevolution.Itshouldbecome
pyriteorothercrystalsmaycarryFe–S-clusters,akinto
clearasthetextproceedsthatthepioneerorganismisa
thoseinFe–S-enzymes(Wa¨chtersha¨user1992),which
chemically deterministic entity at the threshold
may include other transition metals. This holds for all
betweenthe abiotic worldandthe bioticworld.
crystals in the progression, like mackinawite that has
In the years following the first publication of the
been detectedin FeSprecipitatesafter partialreaction
iron–sulphur-world theory, a number of experimental
with H S to pyrite (Drobner et al. 1990). Amorphous
resultshavebeenobtained.Theywillbereportedlater. 2
FeS precipitates have been found to consist of
Sufficeittosayherethattheseexperimentshaveledto
nanocrystalline mackinawite (Michel et al. 2005).
significant improvements of this developing theory.
Greigite has been considered as an intermediate
The theoretical–experimental research programme
(Popper 1990) and as catalytic species (Russell et al.
has, as its ultimate goal, to reconstitute the pioneer
2003,2005).
organism andwatch it evolve.
The organic compounds of the superstructure arise
We turn first to a general characterization of the
byreductivecarbonfixation,i.e.byredoxreactions,for
pioneer organism (figure 1). It has a minimal
whichliquidwaterisbeneficialratherthandetrimental.
substructure–superstructure organization. The super-
The redox reactions are catalysed by the transition
structure consists of low-molecular bioorganic metal centres in or on the surfaces of the inorganic
compounds. They are bonded to the surfaces of an substructure.Theorganiccompoundsbecomebonded
inorganic substructure, i.e. as an interphase between to the substructure in statu nascendi, i.e. as ligands to
the inorganic substructure and the water phase. I use the transition metal centres in the surface of the
here the name pioneer organism for the totality of the substructure. They subsequently undergo lateral
organic molecules that are bonded at any given time transfer. In order to understand the mechanism of
to the inorganic surfaces plus the surface regions of lateraltransfer,wehavetoappreciatetheomnipresence
the inorganic substructure. Extension and curvature ofwater.Thewatermoleculesoccupyall‘free’valences
of the surfaces of the substructure are indefinite. In in the surface of the substructure and any lateral
the direction normal to the inorganic surfaces, the transfer of a ligand involves replacement of water
superstructure has an essentially monomolecular molecules. For a closer understanding of the
extension and a vectorial orientation. The water mechanism of lateral transfer, we have to introduce
phase constitutes the environment and the source an important terminological distinction. The ligands
of nutrients. thataredirectlybondedtothetransitionmetalcentres
The inorganic substructure may form in a great are termed ‘inner sphere’ ligands and those that are
varietyofways,whichpresentlycannotbeexhaustively separated from the transition metal centres by a
defined. Three aspects of substructure formation number of water molecules are termed ‘outer sphere’
deserve special mention and they are asfollows: ligands.Therefore,alateraltransferofaligandinvolves
transfer from the inner sphere to an outer sphere of a
(i) Precipitationfromsolutionmayoccurpriortoor first site, diffusion from the first site to a second site,
duringtheestablishmentofthepioneerorganism. andtransferfromanouterspheretotheinnersphereof
It has been experimentally ascertained earlier the second site. The constituents that detach by
Phil.Trans.R.Soc.B(2006)
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Volcanic origin of chemoautotrophiclife G. Wa¨chtersha¨user 1789
diffusing or flowing into the vast expanses of the open crystals that accretion, core–mantel differentiation
water (ocean) are irretrievablylost. and crust segregation proceeded rapidly and partly in
Such a pioneer organism may be seen as having a parallel (Kleine et al. 2002; Yin et al. 2002; Jacobsen
remarkable combination of three capabilities: for 2003; Harrison et al. 2005). These processes were
growth, reproduction and evolution. These central followedasearlyas4.4Gyr,byoceans,continentsand
aspects of life coincide in the pioneer organism within sedimentation (Mojzsis etal.2001;Wilde et al.2001).
onesingle typeofprocess.Thisprocess maybebriefly This new view extends the time frame for a possible
stated as follows. The thermodynamic driving force is origin of life deep into the Hadean. According to this
provided by the chemical potential of the volcanic emerging picture, a very hot magma and a relatively
exhalationsinthewaterphase.Thekineticreactivityis thin crust (de Wit 1998; Nisbet & Fowler 2004;
providedbythecatalyticactivityofthetransitionmetal Russell & Arndt 2005) would have been highly
centres in or on the surfaces of the inorganic reducing and inflicted by heavy bombardment and by
substructure. The combination of these thermo- intense volcanism with highly reducing exhalations. It
dynamic and kinetic aspectshas the following effects: isexactlythisrangeofconditionsoftheHadeanEarth
thatarecrucialfortheiron–sulphur-worldtheoryofthe
(i) Synthetic carbon fixation reactions generate origin of life.
organic products that become bonded to the In recent years, several remarkable geological
surfaces of the inorganic substructure in statu habitatsfor the origin of life havebeen suggested:
nascendi,which means growth.
(ii) Some of the synthetic organic products exhibit (i) Nisbet & Fowler (2004) suggest localized sites
an autocatalytic positive feedback into the of origin in magnesium-rich komatiite lava
synthetic reactions whence they arise, which deposits associated not only with iron but also
means reproduction. with nickelsulphide.
(iii) The autocatalytic feedback effect exhibits vari- (ii) Nisbet&Fowler(2004)furthersuggestalkaline
ations, which is the basis for evolution. hydrothermal systems or alkaline volcanism as
the most likely setting, where ultramafic
Before we consider the pioneer organism in greater
material (generating magnesium hydroxide)
detail, we may look at the possible geochemical
would be the sourceof alkali.
situationwherein this organism mayarise andthrive.
(iii) Cockell (2006) suggests that large impactors,
long considered a source of heat-sterilization
and as anathema for life, may actually have
3.THE OVERALL GEOCHEMICAL SITUATION prepared the cradle of life by impact cratering.
OFTHE PIONEERORGANISM Thereby intense fracturing and deposition of
Theproblemoftheoriginoflifeisabiologicalproblem dust and debris would have created a bottom
andits solution will be abiological theoryin the sense bed with myriads of flow channels close to the
thattheexplanandumconsistsofextantbiologicalfacts. magmatic source of the volcanicexhalations.
This means that a theory of the origin and the early (iv) Nisbet & Fowler (2004) suggest with regard to
evolution of life will be a biomolecular theory. Its cataclysmic large impacts that primitive life
development should be guided by judging its explana- forms may have survived events of the magni-
tory power (Popper 1963), i.e. its power to explain tude of the Moon-forming impact by being
many facts of extant biology with few theoretical contained in ejected rocks, which then orbited
assumptions. From a chemical point of view, the highinspaceandoutsideofthehotatmosphere
empiricalmeritofsuchatheoryresidesinitspredictive for a sufficient time for later re-entry after the
power, i.e. its power to predict hitherto unknown Earthhad cooled down again.
chemical reactions that can be tested experimentally.
Chemical thermodynamics, as explored by Amend & These proposals are highly compatible with the
Shock (2001), serves to focus the experimental theoryofachemoautotrophicoriginoflifeaspresented
programme. The kinetic issues of the programme can here, which assumes high pressure (Wa¨chtersha¨user
only be resolved experimentally. 1988d,1992),elevatedtemperatures(aboveoraround
Turningnowtotheroleofgeology,itisunfortunate 1008C),(Fe,Ni)-catalysisandthechemicalpotentialof
that we do not have any remains of the Hadean Earth volcanicexhalations.
with a direct biological signature. Therefore, the aim Letusnowaddresstwospecificaspectsofapossible
here can only be the establishment of compatibility cradleoflifewithintheHadeanhabitatsthathavebeen
betweenatheoryoftheearlyEarthandatheoryofthe characterizedearlier:hydrothermalsystemsandvolca-
origin and early evolution of life. Nisbet & Fowler nic exhalations. These two aspects frequently occur
(2004)haveassignedtothegeologiststherole‘topoint side by side and are often confounded. The hydro-
outpossiblehabitatswherethefirstlifecouldhavebeen thermalsystemsarecyclic.Oceanwatercyclesthrough
born’. Efforts in this direction promise the much the crust transporting heat and leached soluble salts
needed constraints of the physical and chemical fromthecrustintotheocean.Fortheoriginoflifethey
parameters for the experiments. areoflesserimportance.Volcanicexhalationsarelinear
There are several reviews of recent theories on the andhenceprimary,virginmagmaticgases(H O,CO ,
2 2
early history of the Earth (Halliday 2004; Russell & CO,H S,etc.)escapeasvolcanicexhalationsfromthe
2
Arndt 2005; Lunine 2006). It now appears from interiorofthemantle.These,uponcooling,providethe
isotope studies of meteorites and Hadean zircon chemicalpotentialfortheoriginoflife.Therefore,they
Phil.Trans.R.Soc.B(2006)
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1790 G. Wa¨chtersha¨user Volcanic origin of chemoautotrophic life
formanindispensablepartofthepresenttheory,which organism. This renders the chemo-autotrophic origin
means that the original homestead of life is situated oflifealocalaffair(Wa¨chtersha¨user1988d)asopposed
in a volcanic flow system (Wa¨chtersha¨user 1988d). tothe globalaffair of the prebiotic broth theory.
A Hadean volcanic flow system may be conceptually
classifiedinto three idealtypes offlowregions:
4.THE BASIC CHEMICAL CONDITIONS OF
(i) A first upstream flow region (deep inside the THE PIONEER ORGANISM
Earth) with a temperature above the critical ThegeochemicalsettingoftheHadeanEarthsuggests
temperature of water may be likened to a flow averygeneralchemicalframeworkforavolcanicorigin
reactor with a stationary solid structure, a oflife.Regardingmorespecificchemicalconditionsof
mobile gas phase and perhaps entrained solid the pioneer organism, we have to rely on a different
particles. It would be the source of the gaseous heuristic:biochemicalretrodictionfromextantbiology.
nutrients for the pioneer organism. Four pointsconsideredhere are asfollows:
(ii) A second downstream flow region with a
temperature below the critical temperature of (i) As to the source for carbon atoms, the extant
water may be likened to a trickle-bed reactor biosphereisbasedmainlyonCO fixation.There-
2
with a stationary solid structure, a mobile gas fore, CO was originally considered as the least
2
phase and a mobile liquid water phase with speculativecandidateandCOwasconsideredasa
dissolvedvolcanicexhalations.Thewaterphase possiblealternative(Wa¨chtersha¨user1988d,1990,
progressively condenses in gas flow direction 1992). In the meantime, based on experimental
beginning perhaps as a thin transient film that results,theemphasishasshiftedfromCO toCO,
2
merely wets the solid surfaces and ultimately which makes good chemical, biological and
forming a liquid flow concurrent or counter- geochemical sense. CO is highly reactive and in
current to the gas flow. Additional nutrients extant organisms, it has three central biological
would have been formed here by reactions functions: as the carbon source for acetyl-CoA
dependent on the presence of liquid water;and synthase; as the electron source for carbon
theformationof anorganicsuperstructuremay monoxide dehydrogenase (CODH); and as the
havealreadybegunhere. ligand in all the three hydrogenases (Pierik et al.
(iii) A third flow region with a lower temperature 1999; Lemon & Peters 1999; Lyon et al. 2004).
maybeachromatographicreactorwithapacked Some extant organisms use CO as sole carbon
bed of solid debris or particles, in which a source (e.g. Rother & Metcalf 2004; Wu et al.
mobile liquid water phase passed through a 2005). This, however, seems to be a derived
myriad of flow channels that opened into the feature, since these organisms employ the usual
ocean.ThethirdflowregionmayexhibitpHor CO reduction pathways fed by the CO that is
2 2
sulphidization zoning and chromatographic producedbyoxidationofCO.Finally,COistoday
characteristics for the organic products in the omnipresent in volcanic gases and the Hadean
superstructure.Itmeansthattheconstituentsof volcanicgaseswouldhavehadahighratioofCO:
the surface metabolism may have been selected CO . In addition to CO and CO, volcanic
2 2
by differential residence times, which means carbonylsulphide(COS;Corazza1986)hasbeen
differentialretentiontimesinviewofthestateof considered as nutrient (Wa¨chtersha¨user 1992).
volcanic flow. Reactive and chromatographic Cyanoligandsoccurringatvolcanicsites(Mukhin
processes would have interacted along the flow 1974)andintwoofthethreehydrogenasesarealso
pathwithbestsurfacebondersbeingtheslowest possiblenutrients.
travellers. (ii) As to the source of reducing power, a number of
inorganicsourcesofelectronshavebeensuggested
Geochromatographyhasbeenpreviouslyinvokedin thatexisttodayandmusthavealwaysexistedunder
conjunctionwithaprebioticbroth(Wing&Bada1991, volcanicconditions:
2000) or with aquifers (Washington 2000). Corliss —oxidative formation of pyrite (Wa¨chtersha¨user
(1986)hasanalysedpossibleflowreactorconditionsof 1988b),
a submarine hydrothermal vent. Subsequently, a FeSCH S/FeS C2HCC2eK; ð4:1Þ
2 2
number of other geologists have explored possible
—oxidation of CO to CO (Wa¨chtersha¨user
Hadean/Archaean hydrothermalvent scenarios for the 2
1988d,1998a),
origin of life (Russell et al. 1989, 1998, 2003, 2005;
COCH O/CO C2HCC2eK; ð4:2Þ
Holm 1992; Matsuno 1997; Russell & Hall 1997; 2 2
Holm & Andersson 1998;Shock et al.1998). —oxidation of ferrous compounds, like ferrous
The involvement of volcanic exhalations in the hydroxide(Huber&Wa¨chtersha¨user2003),
originoflifehasbeeninvokedasearlyas1974(Mukhin 2FeðOHÞ /2FeOðOHÞC2HCC2eK; ð4:3Þ
2
1974).Mukhinsuggestedvolcaniccarboncompounds
—oxidationofH (Wa¨chtersha¨user1988a,c,d),
as an additional source for the synthesis of organic 2
compounds for the ‘prebiotic broth’. The present H2/2HCC2eK: ð4:4Þ
theoryof a chemoautotrophic origin of life utilizes the Thetwohalf-reactions(4.1)and(4.2)withpyriteand
volcanic flow system in a quite different manner. It is CO aswasteproductsarethetwomostcrucialelectron
2
firstofallthesiteatwhichthepioneerorganismarises. donorsforthepioneerorganism.Half-reaction(4.4)has
Inaddition,itprovidesallthenutrientsforthispioneer been ‘excluded as the first source of electrons since its
Phil.Trans.R.Soc.B(2006)
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Volcanic origin of chemoautotrophiclife G. Wa¨chtersha¨user 1791
reducing potential is not sufficient for reducing CO ’ —FormationofCOSfromCOandH SbyNi-catalysis
2 2
(Wa¨chtersha¨user1988d),butnotasafurthersourceof (Huber&Wa¨chtersha¨user1997).
electrons.Thehalfreaction(4.1)hasbeendemonstrated COCH S/COSC2HCC2eK: ð4:7Þ
2
as viable source of electrons for the reduction of CO
2 —Formation of methylmercaptan from CO with
(Heinen&Lauwers1996),whichmeansCO -fixationby 2
2 FeS/H S(Heinen&Lauwers1996).
oxidative pyrite formation. As a peculiar aspect of 2
CO C3FeSC4H S/CH SHC3FeS C2H O:
biomineralization, it has been discovered that the 2 2 3 2 2
conversion of greigite to pyrite may be inhibited by ð4:8Þ
aldehydes (Rickard et al. 2001). Pyrite chemistry, in —FormationofmethylmercaptanfromCOandH Son
2
conjunction with chemical origin of life reactions has NiS(Huber&Wa¨chtersha¨user1997).
beenreviewedbyCody(2004).Thesurfacebondingof
COCH SC4eKC4HC/CH SHCH O: ð4:9Þ
pyrite has been studied, notably by Schoonen and 2 3 2
co-workers, who found strong bonding of phosphate 5.SYNTHETICREACTIONSOFTHEPIONEER
and phosphorylated compounds to pyrite (Bebie & ORGANISM
Schoonen1999). We now turn to synthetic reactions that begin with
simple volcanic nutrients and produce low-molecular
(iii) As to the source of sulphur, volcanic H S, the
2 organic compounds. We should bear in mind that the
simplest of all sulphydryl compounds, has been
reactions are catalysed by metal centres in or on the
consideredasanessentialnutrientandcatalystof
surface of the inorganic substructure. We shall
the pioneer organism and for generating FeS,
progress in the direction of increasing molecular
FeS andother transition metalsulphidesinthe
2 complexity.
substructure(Wa¨chtersha¨user1988b).
(iv) Finally, as to the nature of the transition metal
(a)FormationofC2-structures
centres of the inorganic substructure, extant
The formation of activated thioacetic acid (CH –CO–
3
metallo-proteins suggest first and foremost Fe,
SH)fromCH SHandCOasevolutionaryprecursorof
3
whichisthemostabundanttransitionmetalofthe
acetic acid thioesters was suggested theoretically
Solar System. Ni is a most important catalytic
(Wa¨chtersha¨user 1990). The formation of acetic acid
metalofBacteriaandArchaeaanditisthesecond
and its thioester was demonstrated experimentally at
most abundant transition metal of the Solar
1008C(Huber&Wa¨chtersha¨user1997):
SystemandaconstantcompanionofFe.There-
fore,ithasbeensuggestedearlier(Wa¨chtersha¨user 2CH SHCCO/CH –CO–S–CH CH S: ð5:1Þ
3 3 3 2
1988d, 1990, 1992) and tested experimentally
Thearithmeticissimple:C1CC1ZC2.Thereaction
(Huber & Wa¨chtersha¨user 1997, 1998). The
is catalysed by (Fe,Ni)S, NiS, Ni(OH) and CoS. It
other biological transition metals, namely Mn, 2
combinesstructureformationwithenergyconservation
Co,Mo,W,Cu,ZnundVmayalsobeconsidered.
as group activation energy required for subsequent
The suggestions for possible ligands are derived
reactions.Thereactionresemblestheextantacetyl-CoA
from the ligands of extant metallo-proteins, e.g.
biosynthesis.
S, SH, S–S, H O, OH, CO and CN. These
2
possiblemetalsandligandscombinetoarichset
(b)FormationofC3-structures
of possible inorganic structures within a precipi-
The formation of pyruvate by CO-fixation was
tate (library) of polynuclear, polymodal and
suggested theoretically (Huber & Wa¨chtersha¨user
heteroleptic clusters on mineral surfaces
1997) and demonstrated experimentally at 2000bar
(Wa¨chtersha¨user2000a,b).
and2508CwithFeS/RSH(Codyetal.2000):
Thesereactantssuggestanumberofsimple,testable 3COC4HCC4eK/CH –CO–CO–OH: ð5:2Þ
reactions of volcanic nutrients in the formation and 3
growthofapioneerorganism.Thesereactionsmaytake The arithmetic is C1CC1CC1ZC3. In extant
place at the site of the pioneer organism for immediate biochemistry,pyruvateisformed byreductive carboxy-
infiltration into its surface metabolism or upstream lation of acetyl-CoA, seen here as the evolutionary
thereof with subsequent transport of their products to successorreaction.
thesiteofthepioneerorganism.Thefollowingreactions
havebeenexperimentallydemonstrated: (c)Reductiveamination
Reductiveformationofa-aminoacidsfroma-ketoacids
—FormationofdihydrogenfromFeS/H2S(Tayloretal. and NH3 was suggested (Wa¨chtersha¨user 1990) and
1979;Drobneretal.1990). demonstratedat1008C(Hafenbradletal.1995;Huber
&Wa¨chtersha¨user2003):
FeSCH S/FeS CH : ð4:5Þ
2 2 2 R–CO–COOHC2Fe2CCNH C2HC/
3 ð5:3Þ
—Nitrogen fixation with FeS/H2S under moderate R–CHðNH2Þ–COOHC2Fe3CCH2O:
conditions suggested theoretically (Wa¨chtersha¨user
The reaction proceeds with FeS and/or Fe(OH) as
1988d) and demonstrated with 15N–N (Do¨rr et al. 2
2 catalystandelectronsourcesuggestingtheoxidationof
2003). Fe2C to Fe3C as primary electron source, followed by
N C3FeSC3H S/3FeS C2NH : ð4:6Þ the formation of FeS2 in the presence of H2S or of
2 2 2 3
FeOOH, Fe O , Fe O , etc., in the absence of H S.
2 3 3 4 2
Phil.Trans.R.Soc.B(2006)
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1792 G. Wa¨chtersha¨user Volcanic origin of chemoautotrophic life
protein hydrolysis. In competition with N-terminal
ATP
hydantoin formation, the free amino group of the
dipeptidemayreactwithanothermoleculeofaminoacyl
N-carboxyanhydride to form a tripeptide, which again
O
H2C Gly HOOC–NH–CH CO–NH–CH –COOH may react competitively by N-terminal chain extension
HN N O 2 2 to a tetrapeptide or by N-terminal derivatization and
CO degradationandsoon.Thepeptidecyclemaybeseenas
O 2
acatalyticcyclefortheconversionofCOtoCO akinto
H N–CH –CO–NH–CH –COOH 2
[2H] 2 2 2 extantCODH.Thepeptidecyclewillrunaslongasthe
CO redoxenergysupplyofCOlasts.H Siscatalyticforthe
CO 2
[2H]
formation of COS. The hydrolytically sensitive COS is
(Fe,Ni)S merely an intermediate and its accumulation is not
O
gly H C required.Withadditionalaminoacids,peptides(hydan-
2
H toinsandureas)withavarietyofsequencesareformed
HN N–CH –COOH
CO +H O 2 tocoexistinmixture.Thisconstitutesadynamiclibrary,
2+H2O H2C–COOH 2 O inwhichthepeptides(hydantoinsandureas)comeand
HN NH–CH –COOH purines gowithsteady-stateconcentrationscorrespondingtothe
2
difference between the rates of formation and
O
degradation. Importantly, this library of structures is
Figure2.Dipeptidecycleofglycine.Forpossiblealternatives also self-selecting, because a selective bonding of a
see Huber & Wa¨chtersha¨user (1998) and Wa¨chtersha¨user
certain structure as ligand to a metal centre of the
(1998a).
substructure causes its stabilization against hydrolysis
Glutamate synthase, one of the extant enzymes for and thus an increase of its steady-state concentration.
reductive amination still depends on FeS-clusters for Thismeansaself-selectionofstablemetallo-peptides.
electrontransport.
(e)Phosphorylation
VolcanicgasescontainvolatileP O ,whichhydrolyses
(d)Activationofaminoacidsandpeptidecycle 4 10
through intermediate polyphosphates and pyro-
Amino acid activation and peptide formation were
phosphate (Yamagata et al. 1991) that function as
discovered when a-amino acids were added to the
phosphorylation agents, i.e. as inorganic substitutes for
reactionsystemforformingthethioesterof aceticacid.
ATP (Baltscheffsky 1967). Pyrophosphate has been
Inthepresenceof(Fe,Ni)S,COandH S(orCH SH)
2 3 suggested as primordial phosphorylation agent
at 1008C, the reaction proceeds best under alkaline
(Baltscheffsky 1971). Extant organisms produce pyro-
conditionswith Mg(OH) aspHbuffer.COSwasseen
2 phosphate by photo-phosphorylation (Baltscheffsky
as the activating intermediate, since its use instead of
et al. 1966). Under standard temperature and pressure
CO also produces peptides (Huber & Wa¨chtersha¨user
conditions, COS activates amino acids to subsequently
1998).ActivationwithCOSintheabsenceof(Fe,Ni)S
reactwithAMPtoaminoacyl-AMPandwithphosphate
was studied at room temperature (Leman et al. 2004).
toaminoacyl-phosphate,whichsubsequentlyreactswith
Peptides formed with CO were shown to undergo
further phosphate to pyrophosphate (Leman et al.
N-terminal conversions, first to a hydantoin ring and
2006).
thentoaureagroup,fromwhichfinallytheN-terminal
The aforementioned synthetic reactions may
aminoacidiscleavedhydrolytically(Huberetal.2003).
combine to autotrophic synthetic pathways. A pathway
Ahypotheticalmechanismoftheentirepeptidecycleis
example progressing from CO to the peptide cycle is
shown infigure2 for the simplestcaseofthedipeptide
shown in figure 3. The reactions demonstrated so far
glycyl–glycine.Inthefirststep,glycine(Gly)isactivated
may well be the tip of an iceberg of synthetic reactions
to its aminoacyl N-carboxyanhydride (N) by reaction
forapossiblepioneerorganismwaitingtobediscovered
withCOSobtainedfromCOandH S.Thismeansthat
2 experimentally.
the redox energyof reaction (4.3) is coupled to glycine
activation via COS, which may well be the simplest
pioneerenergycouplingoflife.Subsequently,theamino 6.THEPIONEERMETABOLISM,ITS
group of another molecule of glycine reacts as a REPRODUCTIONANDEVOLUTION
nucleophile with the aminoacyl N-carboxyanhydride (a)Metabolismbyligandfeedback
generating the dipeptide glycyl–glycine, which then We next turn to mechanisms by which the synthetic
reacts at its N-terminal end with COS (CO/H S) reaction pathways in the superstructure of the pioneer
2
generating hydantoin (H) as N-analogue of the organism may exhibit autocatalytic feedback, which
N-carboxyanhydride(N). wouldmeanmetabolicreproduction.Wefirstnotethat
Uptohere,thepeptidecycleissyntheticoranabolic. growth of the superstructure refers to an accumulation
The subsequent hydrolysis to a urea derivative is still of surface-bonding products. These products must be
anabolicsincethemolecularweightincreases.Thefinal seen as ligands to the free metal valences in or on the
hydrolytic cleavage is catabolic and reminiscent of the surfacesoftheinorganicsubstructure.Atthisinstance,it
extantNi-enzymeurease.Thecombinationof anabolic is important to recognize that some of these catalyst
and catabolic cycle segments corresponds to the ligands may increase the catalytic activity of the
extant combination of ribosome-catalysed, anabolic transition metal centres, to which they are bonded.
protein synthesis with proteasome-catalysed, catabolic Thisinturnwouldincreasetherateofthepathwaythat
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Volcanic origin of chemoautotrophiclife G. Wa¨chtersha¨user 1793
metal centre. Let us further assume that this ligand
volcanic exhalations
increasesthecatalyticactivityforarate-determiningstep
CO + H S + NH
2 3 inthereactionpathwaytothisspecialreactionproduct.
This means that the overall rate of this pathway is
CH
3 increased. As a consequence, the steady-state concen-
CO
trationofthespecialreactionproductisincreased.This
CH
OH 3 in turn means that the rate of this pathway is further
+ CO CH3 increased, etc. This is how an autocatalytic feedback
CH3 CO CHNH2 works.Atthisinstance,however,wehavetoappreciate
CO OH CO thattheautocatalyticpathwaygeneratesnotjusttheone
CH
3
SCH OH special reaction product, but rather a whole set of
SH 3
reaction products, e.g. a set of peptides, hydantoin
CH
O 3
derivatives and urea derivatives. This means that the
CH CO
C 3 peptide autocatalytic feedback effect of the one special product
CH3 CO CO Ala cycle increases the steady-state concentration of each
S
compound in the set of reaction products. This brings
the steady-state concentrations of some other products
FeS NiS FeS NiS FeS NiS up to levels, at which further feedback possibilities are
actualized. In this manner, a single positive feedback
ligand feedback effect will broaden the spectrum of products, which in
Figure 3. Integrated hypothetical reaction pathway with turn will usher in further feedback effects. This means
autocatalyticfeedback(dottedarrows). that the metabolism of the pioneer organism is self-
expanding and undergoing a progressive increase of
producestheligand(Wa¨chtersha¨user1998a,c,2000a,b; metabolic diversity and molecular complexity, thus
cf.Huber&Wa¨chtersha¨user1998).Suchligandeffects exhibiting an ever-expanding avalanche of metabolic
are quite idiosyncratic and theoretically not very evolution.
predictable (Berrisford et al. 1995). Carefully chosen Let us finally consider reproduction and evolution
ligands may dramatically increase the activity of undertheflowconditionsofachromatographicreaction
transitionmetalcatalystsbyfactorsofupto103. system. Strong-bonding products, e.g. certain peptides,
Let us now analyse which kinds of low-molecular have a long retention time and migrate slowly in flow
organic products may become ligands for boosting direction. This means that they tend to become
catalytictransitionmetalcentres.Typically,suchligands concentrated in a relatively early flow zone, which may
willhaveatleasttwofunctionalgroups(e.g.COOHand be termed the ‘ligand zone’. Local concentration of
NH2) that can bond to a transition metal centre. certainligandsinaligandzonemeansalocalizationofthe
Examples are hydroxy acids, e.g. glycolate, lactate, feedbackeffectoftheligands.Thisinturnincreasesthe
glycerate, malate, citrate, isocitrate and homocitrate, rateofreactionintheligandzoneandthustheproduction
the latter being a ligand in extant nitrogenases (Kirn & of more ligandsand still stronger feedback in this zone.
Rees1992;Ru¨ttimann-Johnsonetal.2001);aminoacids, Thismeansconcentrationandlocalizationofthepioneer
e.g. glycine, alanine, serine, aspartate; and peptides or organisminspiteofthevolcanicflowsituation.
theirhydantoinandureaderivatives.Apossibilityofsuch
productfeedbackisindicatedinfigure3. (b)Evolutionbydoublefeedback
We may conceptualize ligand feedback from a Another, not yet discussed, however, crucial aspect of
different point of view. All products of the surface evolutionisbasedonamechanism,whichIhavetermed
metabolism form a mixture (or library) of chemical ‘double feedback’ (Wa¨chtersha¨user 1992, 1994). For
compounds.Somemaybondtothesurfacemoreorless understanding this mechanism, let us assume the pre-
stronglyandothersmaynotbondatall.Presently,from existence of a pioneer metabolism with a specific
this library, the pioneer organism will automatically reaction pathway having a specific product that feeds
select those compounds, which are capable of bonding back autocatalytically into the metabolism. We further
as ligands by selective residence or retention time; and assumethattheself-expansionofthemetabolismbrings
optionally by protection from hydrolysis. In this sense, forthanewreactionpathway,whichbranchesfromthe
the products of the pioneer metabolism are self- specific reaction pathway and thus weakens it, since it
selective. Increase in the size of the library of products withdrawsanintermediate.Now,ifaproductofthenew
increases the likelihood that it contains self-selecting branch pathway feeds back autocatalytically into this
ligands with autocatalytic feedback. Incidentally, from very same new branch pathway, the weakening of the
thispoint ofview,racemates ofthe organic productsof pre-existent specific reaction pathway is amplified.
the pioneer metabolism mean a higher number of Thus, a feedback which is positive (autocatalytic) for
structures and thus a higher likelihood of positive thebranchpathwaywillbenegativefor thepre-existent
feedback, which means that at this early stage of life specific reaction pathway and thereby for the whole
lackofenantioselectivityofthesyntheticreactionsisan metabolism. This is an egotistic, virus-like (‘virulytic’)
advantagerather thanadisadvantage. feedback effect that tends to weaken or even kill the
Theseconsiderationsbringustoamostcrucialaspect pioneer metabolism. A completely different situation
oftheself-selectinglibraryofligands.Letusassumethat arises,iftheproductofthenewbranchpathwayexhibits
onespecialreactionproductofthepioneer metabolism a ‘double feedback’, an ‘egotistic feedback’ combined
(e.g. a certain peptide) binds as a ligand to a catalytic with an ‘altruistic feedback’. The egotistic feedback
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1794 G. Wa¨chtersha¨user Volcanic origin of chemoautotrophic life
consists of the positive feedback into the new branch must have originated by carbon fixation. Various more
pathway. The altruistic feedback consists of a positive or less vague synthetic possibilities have been explored
feedback into the pre-existent metabolism, thereby theoretically (Wa¨chtersha¨user 1988a,d, 1992). The
compensating for the egotistic feedback. The reaction peptide cycle shown in figure 2 now adds surprisingly
productswithsuchadoublefeedbackeffectaretermed direct experimental evidence. The hydantoin rings are
‘vitalizers’ (Wa¨chtersha¨user 1992, 1994). There are formed at the N-terminal ends of peptides by carbon
numerous examples for such vitalizers in extant fixation. Such hydantoin rings have a close structural
metabolism. The coenzymes catalyse many reactions similaritytotheimidazoleportionofthepurinebasesin
including reactions within their own biosynthesis. The extantnucleicacids.Thepurinesaretodatebiosynthe-
ribosomescatalysethesynthesesofallproteinsincluding sized by pathways involving carbon fixation. This
ribosomal proteins. The protein translocases catalyse suggests that in the extant biosynthesis of purines, the
the incorporation of numerous membrane proteins mostancientmannerofsynthesisbycarbonfixationhas
into membranes, including the proteins of the translo- been somehow preserved. Further, this experimental
cases themselves. The principle of double feedback result brings the two ancient syntheses of peptides and
holdsatalllevelsofevolutionfromthepioneerorganism purines into a close connection and it lends support to
through nucleic acid-implemented evolution to the thepossibilitythatamongtheearliest‘nucleicacids’may
evolution of the highest forms of human institutions have been chemoautotrophically produced
(Wa¨chtersha¨user1992,1994). polypeptides with pendant hydantoin-derived bases
(cf. Nielsen 1993). Such primitive ‘nucleic acids’
(c)Metabolicinheritance would have been followed later on by phospho-sugar-
Thechemicalreactionsaredependentonthe(environ- basednucleicacids.
mental)reactionconditions.Bypositivefeedback(single Thestructuralandfunctionalpropertiesofthegeneral
ordouble)oftheproductofareactionintothisreaction class of nucleic acids with a sugar-phosphate backbone
itself, this dependence is lessened compared to the have been intensely studied both theoretically and
feedback-free de novo reaction, which means that the experimentally by Albert Eschenmoser and his school.
reactionbecomestoacertaindegreeindependentfrom Itwasfoundthata-threofuranosyloligonucleotideswith
the environment, i.e. autonomous. This means that an vicinallyconnected(30/20)phosphodiesterbridgeshave
autocatalytic feedback reaction, once initiated de novo, similar base-pairing properties as RNA. Moreover, they
will continue to run even under conditions, which no formhybridswithRNAandDNA,whichisanecessary
longer allow its de novo initiation. This is how history condition for an intermediary evolutionary role. Most
enters the picture. The existence of an autocatalytic importantly, however, they show a much increased
feedback cycle signifies the historic fact of its previous hydrolytic and thermal stabilities compared to RNA.
de novo ignition. In this sense, each autocatalytic Finally,theC4-sugarcomponentcouldbetheresultofa
feedbackeffectconstitutesaninstanceofinheritanceor C2CC2/C4 synthesis (Scho¨ning et al. 2000). This
amemoryeffectandthewholeprocessofevolutionmay makesitagoodcandidateforanucleicacidoriginatingin
beabstractedtoaconcatenationofsuchmemoryeffects. a hot chemoautotrophic system. In this context, the
problemisfurtherconstrainedbyaddingtothecategories
of structural and functional feasibility, the metabolic
7.ONTHECHEMOAUTOTROPHICORIGIN categoryofautotrophicsyntheticaccessibility.Thisisstill
OFTHEGENETICMACHINERY alargelyunchartedterritory.Onecrucialproblemwithin
So far, we have discussed the hypothetical pioneer this territory, the problem of phosphorylation and of
organismasachemicalentitycontrolledbytheuniversal activation of nucleotides by phosphoanhydride forma-
lawsofchemistry.Wenowinvestigatehowthischemical tion,hasbeenrecentlyaddressedexperimentally(Leman
entitycouldhavebeenthestartingpointoftheparticular et al. 2006). As explained earlier, this solution is quite
historic process of evolution, by which the chemoauto- compatible with the context of a chemoautotrophic
trophicpioneerorganismevolvedintoorganismswitha origin of life and a potential solution of the problem of
genetic machinery. This must have happened in nucleicacidsynthesisbynucleotidecondensation.
coevolutionwithcellularization,whichwillbeaddressed Any solution of the problem in the synthesis of
later. It should be stressed at the outset that there is a nucleicacidsinachemoautotrophiccontextwillhaveto
huge body of literature on the problem of the origin of address not only the question, how the synthetic
genetic machinery in the context of a cold prebiotic intermediates, like phosphorylated sugars, could have
broth. Naturally, much of this work is not directly been formed by carbon fixation, but also the question
applicable to the context of a chemoautotrophic origin howsuchintermediatescouldhaveoperatedasfeedback
under hot, volcanic conditions. Therefore, we will componentswithinanautocatalyticmetabolicnetwork.
restrict the present discussion to certain salient aspects The earliest function of phosphorylated sugars and
ofthenewviewoftheproblemthatisforceduponusby nucleotides—long before the advent of base pairing—
the assumption of a chemoautotrophic pioneer musthavebeenthatofligandsforpromotingtransition
organism. metal catalysts. Sugars are excellent ligands. The
Allextantorganismshaveamulti-componentgenetic heterocyclic bases in the early nucleotides would have
machinery consisting partly of proteins and partly of acquired the additional function of acid–base catalysis.
nucleic acids. The nucleic acids consist of structural Finally,withtheadventofbasepairing,athirdcatalytic
units (nucleotide units) derived from phospho-ribose function was added: catalysis of peptide formation by
and heterocyclic bases. According to the theory of a anchimeric positioning of nucleic acids with terminal
chemo-autotrophic origin of life, these structural units aminoacidesters,towhichweturnnext.
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Volcanic origin of chemoautotrophiclife G. Wa¨chtersha¨user 1795
Today almost all the peptides and proteins are theprimary,direct,chemicalmechanismofevolutionby
synthesized by ribosomal catalysis. As a simple specific variation of the synthesis of peptides with direct
modelenroutetotheribosomalmachinery,letusassume autocatalytic feedback became first supplemented and
surface-bonded pro-tRNAs in the form of nucleic acid later increasingly substituted by a secondary, indirect,
hairpinstructuresthatbecameaminoacylatedterminally genetic mechanism of evolution, whereby variations of
byactivatedaminoacids.Letusfurtherassumethattwo replicating nucleic acid sequences led indirectly to
ofthesesurface-bondedpro-tRNAsbecamelocatedside variations of peptide sequences. This transformation
bysideandattachedbybasepairingwiththeirloopstoa led to a step-by-step replacement of primitive metallo-
surface-bondednucleicacidstrandaspro-mRNA.The peptides by more and more complex coded metallo-
resultofthisbasepair-assistedanchimericpositioningis peptides. It was the basis for the admission of more
a more efficient synthesis of dipeptides to be followed diversified amino acids into the system and for the
laterbyoligopeptides.Thisistheorigin of thesimplest establishment and expansion of the genetic code. The
ribosomal machinery consisting of two pro-tRNAs and conclusion seems to be inescapable: the evolution of
one pro-mRNA.It embodies the chemical (as opposed nucleic acid replication and of nucleic acid-catalysed
to organizational) core of the ribosomal process of peptide synthesis must have been intrinsically linked.
translation. Thisconclusionisinsharpestcontrasttoallthenotions
Intheprecedingparagraphs,wehaveaddressedfirst ofaworldofRNAlifewithRNAreplicationandwithout
theformationofnucleicacidsbypolycondensationand translation(cf.Forterre2005).
thenthefunctionofnucleicacidsascatalystsforpeptide Turningnowtotheadventofproteinfolding,wenote
formation. Let us now try to tie these two processes that in the primitive metallo-peptides metal centres
together. We assume that in the earliest phases of servedascatalystsandaselectrontransferagents.With
evolution, these two processes were essentially insensi- the advent of cysteine in the set of coded amino acids,
tive to or non-selective for particular nucleic acid the metal centres of the metallo-peptides acquired an
sequences. Only later, with the appearance of more additional function, namely that of folding
diversified amino acids, and longer nucleic acids and determinants, which operate by a few strong covalent
peptides,thequestionofacontrolofbasesequencesin metal–sulphurbonds.Thismaybeseenastheoriginof
nucleic acids and of amino acid sequences in peptides proteins,whicharedistinguishedfrompeptidesbytheir
came into the picture. Sequence-controlled (template- ability to form folded structures. This means that the
directed) nucleic acid synthesis, whereby a sequence is emergent folded metallo-proteins acquired, from the
copied from an old strand to a new strand of nucleic start, the hyperthermostability that is required by
acid, is called ‘replication’ and sequence-controlled the high temperature of the volcanic environment of
peptide synthesis, whereby a nucleic acid sequence is early life. A few strong covalent bonds were sufficient
copiedintoapeptidesequence,iscalled‘translation’. and the overall sequence fidelity was not critical. Only
We are now in a position to formulate a basic after a sufficient increase of replication fidelity and
question for the origin of life: what was the temporal translation fidelity, proteins could arise that owed their
order in which the two processes of replication and folding stability, not to a few strong covalent bonds to
translation must have emerged. Before we answer this transitionmetalcentres,butrathertothecooperationof
questionfor thechemoautotrophictheory,letusbriefly a multitude of weak non-covalent group interactions.
recalltheanswerasgiveninthecontextoftheprebiotic Only then, the covalent metal–sulphur folding
broth theory (Bada 2004) in order to guard against determinants could disappear opportunistically one by
confusion. It is assumed in the prebiotic broth theory one in an irreversible evolution down the temperature
that a large library of random sequences would have scale(Wa¨chtersha¨user1998c,2001).
beengeneratedandaccumulatedintheprimitiveocean Finally, within the context of a chemoautotrophic
and that ‘by chance, some of these polymers acquired originoflife,thereisnocompellingreasontoassumea
the ability to catalyse their own imperfect self- particularlylatearrivalofDNAandofthesegregationof
replication [and therefore] soon dominated’ . in the theprocessesofDNAsynthesisbyreplicationandRNA
‘overall pool of polymers’ Thus, replication is indis- synthesis by transcription. It is suggested here that the
pensable for converting the polymer chaos of the earlypolymeraseswerenotabletodiscriminatebetween
prebiotic broth into some sort of molecular order. In ribonucleotides for RNA and deoxyribonucleotides for
thisevolutionarycontext,replicationfidelityisseenasa DNA. This means that after the advent of a gene for
value in itself. The process of translation would have ribonucleotidereductase,thetransitionfromreplication
appeared much later. to transcription would simply be controlled by turning
Inthecontextofachemoautotrophicoriginoflife,we ontheproductionofthisreductase.
cometoadrasticallydifferentconclusion.Here,thetwo Incidentally, within the context of a prebiotic broth,
processes of sequence control, those of replication and CarlWoese(1971)suggestedtheoriginoftranslationas
translation, must have become established jointly, by agradual,continuouschangeoverfrommetalcomplexes
coevolution (cf. Lahav 1999), whereby the emergence with polypeptidesof a non-translationally produced set
and evolution of replication slightly trailed the emer- toasimilarsetoftranslationallyproducedpolypeptides
gence and the evolution of translation. Each new withtheinitialbenefitofanincreasedrateofproduction
increment of added potential sequence selectivity of as opposed to the increased sequence fidelity. In a
translation would have served as the functional advan- similar vein, it has been suggested that early on FeS
tage for a subsequent increment of added sequence reacted withnon-translational peptides or proteins in a
fidelityoftemplate-directednucleicacidsynthesis.Inthe prebiotic broth to form catalytic Fe–S proteins (Eck &
courseofthiscoevolutionoftranslationandreplication, Dayhoff1966;Halletal.1971,1974a,b).
Phil.Trans.R.Soc.B(2006)