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On the Origins of Cells Publishedonline 5December 2002 On the originsof cells:a hypothesisfor the evolutionarytransitionsfrom abioticgeochemist ry to chemoautotrophicprokaryote s,and from prokaryotes to nucleatedcells William Martin 1* and Michael J.Russell 2 1 Institut fu¨rBotanikIII, Heinrich-Heine UniversitaetDu ¨sseldorf,Universita ¨tsstrasse1, 40225 Du ¨sseldorf,Germany 2 ScottishUniversities EnvironmentalResearch Centre, Scottish Enterprise Technology Park, Rankine Avenue,East Kilbride, GlasgowG75 0QF, UK ([email protected] ) All life is organized ascells. Physical compartmentation from theenvironment and self-organization of self-containedredox reactionsare themost conserved attributes ofliving things,hence inorganic matter with suchattributes wouldbe life’ s mostlikely forebear. Wepropose that life evolved in structurediron monosulphideprecipitates in aseepagesite hydrothermal moundat aredox,pH and temperature gradient betweensulphide-rich hydrothermal fluid andiron(II)-containing watersof the Hadean ocean floor. The naturally arising, three-dimensionalcompartmentation observedwithin fossilizedseepage-site metal sul- phide precipitates indicatesthat theseinorganic compartmentswere the precursors of cell walls andmem- branesfound in free-living prokaryotes. The knowncapability ofFeS and NiS tocatalyse thesynthesis ofthe acetyl-methylsulphide from carbon monoxide andmethylsulphide, constituentsof hydrothermal fluid,indicates that pre-biotic synthesesoccurred at theinner surfaces of these metal-sulphide-walled compartments,which furthermore restrainedreacted products from diffusioninto the ocean, providing sufficientconcentrations of reactants to forge thetransition from geochemistry tobiochemistry. The chem- istry ofwhat isknown as the RNA-world could have takenplace within thesenaturally forming, catalytic- walled compartmentsto give rise toreplicating systems.Sufficient concentrations of precursorsto support replication wouldhave beensynthesized in situ geochemically andbiogeochemically, with FeS (andNiS) centresplaying thecentral catalytic role. The universal ancestorwe infer wasnot a free-living cell,but rather wasconfined to the naturally chemiosmotic,FeS compartmentswithin which thesynthesis of its constituentsoccurred. The first free-living cellsare suggestedto have beeneubacterial andarchaebacterial chemoautotrophsthat emergedmore than 3.8 Gyr ago from their inorganic confines.We propose that theemergence of these prokaryotic lineages from inorganic confinesoccurred independently, facilitated by theindependent origins ofmembrane-lipid biosynthesis:isoprenoid ether membranes in thearchae- bacterial andfatty acid estermembranes in theeubacterial lineage. The eukaryotes,all ofwhich are ancestrally heterotrophsand possess eubacterial lipids, are suggestedto have arisen ca.2Gyr ago through symbiosis involving anautotrophic archaebacterial hostand a heterotrophic eubacterial symbiont,the commonancestor of mitochondria andhydrogenosomes. The attributes sharedby all prokaryotes are viewedas inheritances from their confineduniversal ancestor.The attributes that distinguish eubacteria andarchaebacteria, yet are uniform within thegroups, are viewedas relics oftheir phaseof differentiation after divergencefrom thenon-free-living universal ancestorand before the origin ofthe free-living chemoautotrophic lifestyle. The attributes sharedby eukaryoteswith eubacteria andarchaebacteria, respectively, are viewedas inheritances via symbiosis.The attributes uniqueto eukaryotes are viewedas inventionsspecific to their lineage. The origin ofthe eukaryotic endomembranesystem and nuclear mem- brane are suggestedto be the fortuitous result of the expression of genes for eubacterial membrane lipid synthesisby an archaebacterial geneticapparatus in acompartment that wasnot fully prepared toaccom- modatesuch compounds, resulting in vesiclesof eubacterial lipids that accumulatedin thecytosol around their siteof synthesis. Under these premises, the most ancient divide in theliving worldis that between eubacteria andarchaebacteria, yet thesteepest evolutionary grade is that betweenprokaryotes andeukaryotes. Keywords: hydrothermal vents;acetyl-CoA pathway; origin oflife; RNA-world; chemoautotrophic origins; holochirality 1. INTRODUCTION *Authorfor correspondence ([email protected]). The Earth is 4.5 billion years (Gyr) oldand the first ocean One contribution of 21to a DiscussionMeeting Issue ‘Chloroplastsand had condensedby ca.4.4 Gyr (Wilde et al. 2001). There mitochondria: functional genomics and evolution’. are goodreasons to believe that life arosehere by ca. Phil. Trans. R.Soc. Lond. B (2003) 358, 59–85 59 Ó 2002 TheRoyal Society DOI 10.1098/rstb.2002.1183 60W. Martinand M. J. Russell On theorigins of cells 3.8 Gyr,because carbon isotopedata provide evidencefor last commonancestor, its attributes canonly beaddressed biological CO 2 fixation in sedimentary rocksof that age through logical inference(Penny & Poole 1999). (Mojzsis et al. 1996; Rosing 1999; Nisbet& Sleep2001; What didthe ancestor of prokaryotes possessfor sure? Ueno et al. 2002). By 3.5 Gyr,stromatolites werepresent, It certainly possessedthe universal geneticcode, tRNA preservedmicrobial mats indicative ofdeposition by pho- (Eigen& Schuster1978; Woese et al. 1990; Eigen1992) tosyntheticprokaryotes (Walter 1983; Nisbet& Sleep andribosomes with abattery ofribosomal proteins 2001). By ca.1.5 Gyr,so-called acritarchs becamereason- (Woese2002), mostof which are neatly encodedin acon- ably abundant,microfossils of unicellular organisms that servedsuperoperon that is presentand conserved in gene are almost certainly eukaryotes( Javaux et al. 2001) and order acrossmany genomes(Wa ¨chtersha¨user1998). Fur- probably algae becauseof an easily preservedcell wall. By thermore, theuniversal ancestorsurely possessedDNA 1.2 Gyr,spectacularly preservedmulticellular organisms (Reichard 1997; Poole et al. 2000) andDNA polymerases, appear that werevery probably redalgae (Butterfield RNA polymerases,and a battery ofaccessory translation 2000). There have beenreports ofmore ancientremains factorssuch as EF-Tu and EF-G that are presentin all claimed tobe eukaryotes, but they are equivocal. For prokaryotes (Poole et al. 1998, 1999), probably along with example Grypania is a2.1 Gyr fossil(Han & Runnegar other more or lessubiquitous prokarytotic proteinssuch 1992), butcould just as easily bea filamentousprokaryote as F1 –F0 -typeATPases (Gogarten et al. 1989) aswell as asa filamentouseukaryote, because the cellular structure prokaryotic forms ofthe signal recognition particle, which ofthefossil is notpreserved. More recently, steranes were is anaccessory to translation (Brinkmann &Philippe foundin 2.7 Gyr sedimentsand were claimed toprovide 1999). Furthermore, it had tohave had all ofthepathways evidencefor theexistence of eukaryotes at that time necessaryfor efficientnucleotide and amino-acid (Brocks et al. 1999), butseveral groups ofprokaryotes biosyntheses,a corecarbon metabolism toprovide the including methanotrophic proteobacteria (seeSchouten et biosynthetic precursors,and the cofactors required for al. 2000), myxobacteria (Kohl et al. 1983) andcyanobac- thosebiosynthetic pathways: butthis is thepoint where teria (Hai et al. 1996) make thesame kinds of compounds things get very complicated very quickly, becausealthough (for example cholesterol)claimed tobe eukaryote-specific, archaebacteria andeubacteria domany things similarly suchthat thesterane evidence for theage ofeukaryotesis whenit comesto the processing of genetic information questionableat best.Ultra-light carbon material that bears (Woese2002), they domany things fundamentally differ- theisotopic signature ofbiological consumptionof bio- ently whenit comesto central metabolism. logically producedmethane goes back to2.7 Gyr (Hayes Onesimple example for suchcore metabolic differences 1994), providing evidencefor thedistinctness of eubac- betweenthe two groups ofprokaryotes is thebreakdown teria (methanotrophs) andarchaebacteria (methanogens) ofglucose to pyruvate, theglycolytic (Embden –Meyerhof) by that time at thevery least,and furthermore indicating pathway, which is universal among eukaryotes,but not that arguments for an origin ofarchaebacteria only among prokaryotes. If welook among prokaryotic gen- 850 million years (Myr) ago (Cavalier-Smith 2002) must omesfor thefamiliar glycolytic enzymesthat occurin be in error. eukaryotes,we see that they have goodhomologues Thosegeological benchmarksprovide rough butrobust among awidespectrum of eubacterial genomes,but many orientation for theprocess of early evolution:the origin of ofthe corresponding homologues are missing in archaeb- prokaryotes by at least 3.5 Gyr andthe origin ofeukary- acteria (figure 1). This observation might seempuzzling otesby at least 1.5 Gyr.But biologists andgeologists alike tosome (Canback et al. 2002) butis easily attributable to wouldlike toknow a fewmore details.What happened twosimple factors.First, although archaebacteria possess during thosefirst 2.5 Gyr? Howdid life get offthe ground pathways from glucoseto pyruvate, they have several alter- tobegin with? Why didit take eukaryotesso long to native pathways that involve differentenzymatic steps, appear? Why are thetwo groups ofcontemporary prokary- hencedifferent enzymes not present in glycolysis otes(eubacteria andarchaebacteria) sogenetically coher- (Daniel &Danson1995; Scho¨nheit & Scha¨fer 1995; entyet sobiochemically different?Why are thereno Kengen et al. 1996; Selig et al. 1997). Theseinclude: (i)
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