30CHAPTER 2FORMATIONOF THE BIOSPHERE:KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTSMaEraPeriod0First humansQuartemaryCenozoicand Tertiary Mammals diversity65 Mass extinction(end of dinosaurs)Sterile EarthCretaceousPrebiotic syntheses→ Rise of flowering(proteins and RNAplantsMesozoicmade abiotically)QJurassicRNAFirst dinosaursFirst mammalsTriassic251Great massThe→extinctionPermianSelf-replicating RNAsRNAOSPennsylvanianworlde8Rise of seedxMississippian001Lipid orplantsPrstandlipoproteinDevonianvertebratesvesiclePaleozoicSlurian First land plantsOrdovicianEarly cellular life(RNAas coding andWCambrianCambriancatalytic molecule)explosion543Phanerozoic EonProtein Early animalsProteins assume catalytic21% ongygen inCellularNeoproterozoicCthe atmospherefunctions(RNAonlyasEralifecoding molecule)1000 Fossil protozoaMesoproterozoicEvolution of DNAEraProterozoic Ozone shieldfromRNA1600DNAEonBanded iron-Modern cellularlife00formationsPaleoproterozoic(DNAreplacesRNAasEracoding molecule leadingto1% oxygen in- te amosphereDNARNAprotein)2500Figure 2.3A general model of biochemicalEarly eukaryotes Cyanobacteriaand biological evolution.ConnectionsArchaenEonbetweensterileprebioticand cellularAnoxygenic-stages of life rely on gradually increasingphotosynthesiscomplexity.Keymilestoneswere chemicalOidest sedimentary-rockssynthesis, surface catalyzed reactions,4000Oldest continentalthe RNA world, the last universalcrustHadeanEoncommonancestral community.andcompartmentalization to form free-living4600 Age of Earthcells.(From MADIGAN,M.and J.Figure 2.2 Geological timescales andMARTINKO.2006.BrockBiology ofevolutionary events.Note that the scale is notMicroorganisms,1lthedn,p.304.Copyrightlinear (Ma, 1o°years ago). (Modified from Knoll)2006,reprintedbypermission ofPearsonA.H.2003.Life on a Young Planet. CopyrightEducation,Inc.,UpperSaddleRiver,NJ.)2oo3,PrincetonUniversityPress.Reprintedbypermission of Princeton University Press.)
30 CHAPTER 2 FORMATION OF THE BIOSPHERE: KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTS Figure 2.2 Geological timescales and evolutionary events. Note that the scale is not linear (Ma, 106 years ago). (Modified from Knoll, A.H. 2003. Life on a Young Planet. Copyright 2003, Princeton University Press. Reprinted by permission of Princeton University Press.) Prebiotic syntheses (proteins and RNA made abiotically) Early cellular life (RNA as coding and catalytic molecule) Proteins assume catalytic functions (RNA only as coding molecule) Modern cellular life (DNA replaces RNA as coding molecule leading to DNA RNA protein) Evolution of DNA from RNA Self-replicating RNAs RNA + Lipid or lipoprotein vesicle Protein DNA Sterile Earth The RNA world Cellular life Ma0 65 First humans 251 543 1000 1600 2500 4000 4600 Era Period Cenozoic Mesozoic Paleozoic Quarternary and Tertiary Cretaceous Jurassic Triassic Permian Pennsylvanian Mississippian Devonian Silurian Ordovician Cambrian Phanerozoic Eon Proterozoic Eon Archaen Eon Neoproterozoic Era Mesoproterozoic Era Paleoproterozoic Era Hadean Eon Mass extinction (end of dinosaurs) Rise of flowering plants Great mass extinction First land plants Cambrian explosion Early animals 21% oxygen in the atmosphere 1% oxygen in the atmosphere Fossil protozoa Ozone shield Banded iron formations Early eukaryotes Cyanobacteria Oldest continental crust Age of Earth Oldest sedimentary rocks Anoxygenic photosynthesis First dinosaurs First mammals Rise of seed plants First land vertebrates Mammals diversity Figure 2.3 A general model of biochemical and biological evolution. Connections between sterile prebiotic and cellular stages of life rely on gradually increasing complexity. Key milestones were chemical synthesis, surface catalyzed reactions, the RNA world, the last universal common ancestral community, and compartmentalization to form free-living cells. (From MADIGAN, M. and J. MARTINKO. 2006. Brock Biology of Microorganisms, 11th edn, p. 304. Copyright 2006, reprinted by permission of Pearson Education, Inc., Upper Saddle River, NJ.) 9781405136471_4_002.qxd 1/15/08 8:47 Page 30
31CHAPTER2FORMATION OFTHEBIOSPHERE:KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTSScienceandthecitizenWar of the Worlds and martian lifeHeadlinenewsfromEnglishliteratureand AmericanradioTHEMARTIANSHAVELANDED!!The1898novelbyH.G.WellsdepictedaninvasionofEnglandbyaliensfromMars.Meteor-like, cylindrical spaceships landed throughout the countryside.Tentacled creatures assem-bledarmedfightingmachinesthatbroughtfearanddestructiontohumanity.In1938,theAmerican writer,director,and actor,Orson Wells (not related to H. G.Wells)broadcast aradio showbased on War of theWorlds.Theradiobroadcast was so realisticthat itcausedwidespreadpanicamongradiolistenersSCIENCE:Real martian life?ContrarytoH.G.Wells andOrsonWells'depictionof sophisticatedmartianswithadvancedtechnology, the real news about extraterrestrial life is microbial. On August 16, 1996, anarticlebyMcKayetal.,entitled"SearchforpastlifeonMars:Possiblerelicbiogenicactiv-ityinmartianmeteoriteALH84oo1"appearedintheprestigiousSciencemagazine.Theauthorshypothesiswasthatmicroorganisms onMars carried outmetabolicactivitiesthatcaused theformation of carbonate globules, magnetite mineral, iron sulfide mineral, and cell biomass.The latter was proposed to have been converted to polycyclic aromatic hydrocarbons (seeSection8.3andBox8.7)duringtransportfromMarstoEarth
CHAPTER 2 FORMATION OF THE BIOSPHERE: KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTS 31 Science and the citizen War of the Worlds and martian life Headline news from English literature and American radio The 1898 novel by H. G. Wells depicted an invasion of England by aliens from Mars. Meteorlike, cylindrical spaceships landed throughout the countryside. Tentacled creatures assembled armed fighting machines that brought fear and destruction to humanity. In 1938, the American writer, director, and actor, Orson Wells (not related to H. G. Wells) broadcast a radio show based on War of the Worlds. The radio broadcast was so realistic that it caused widespread panic among radio listeners. SCIENCE: Real martian life? Contrary to H. G. Wells and Orson Wells’ depiction of sophisticated martians with advanced technology, the real news about extraterrestrial life is microbial. On August 16, 1996, an article by McKay et al., entitled “Search for past life on Mars: Possible relic biogenic activity in martian meteorite ALH84001” appeared in the prestigious Science magazine. The authors’ hypothesis was that microorganisms on Mars carried out metabolic activities that caused the formation of carbonate globules, magnetite mineral, iron sulfide mineral, and cell biomass. The latter was proposed to have been converted to polycyclic aromatic hydrocarbons (see Section 8.3 and Box 8.7) during transport from Mars to Earth. THE MARTIANS HAVE LANDED !! 9781405136471_4_002.qxd 1/15/08 8:47 Page 31
32CHAPTER2FORMATIONOF THE BIOSPHERE:KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTSThe final paragraph of the article summarized the information presented that argued forpast microbial life on Mars.In examining the martian meteorite ALH84oo1 we have found that the following evidence iscompatiblewiththe existenceof past life onMars:(i)an igneous Mars rock (of unknown geologic context)thatwas penetrated bya fluid alongfractures and pore spaces, which then became the sites of secondary mineral formation andpossiblebiogenicactivity:(i) a formation age for the carbonate globules younger than the age of the igneous rock;(ii) scanning electron micrograph and transmission electron micrograph images of carbonateglobulesandfeaturesresemblingterrestrial microorganisms,terrestrialbiogeniccarbonatestruc-turesormicrofossils:(iv)magnetite and iron sulfideparticles that could have resulted from oxidation and reductionreactionsknownto be important interrestrial microbial systems;and(v)the presence of polycyclic aromatic hydrocarbons associated with surfaces rich in carbonateglobules.None ofthese observations isin itself conclusivefortheexistenceof past life.Althoughtherearealternative explanations foreach of thesephenomena taken individually:when they are consid-ered collectively,particularly in view of their spatial association, we conclude that they are evid.enceforprimitivelifeonearlyMars.About 3 years subsequent to McKay and colleague's publication, each of the five argumentsfor ancient martian microbial life was challenged in the scientific literature (e.g.,Anders,1996;Borg etal.,1999).Alternative,largely chemical, mechanisms werefound for thefor-mation of what McKay etal.had argued tobebiogenicstructures.Now,thegeneral con-sensus isthatthishypothesisaboutancientmartian lifehas been disprovenTheintellectualand scientificexerciseof seeking extraterrestrial lifehas,nonetheless,beenbeneficial to environmental microbiology.A new discipline has been born astrobiology.Advances in theastrobiology scientific community have enabled it tobefarbetterpreparedtodocumentnewformsofmicrobiallife.ResearchessayassignmentThe terms"extremophile","exobiology",and"astrobiology"have been used extensively inboththescientificand nonscientific literature.Afterfinding aboutsixpublished works address-ing thesetopics,writea 3-5page essaythatmerges two aspects of astrobiology: (i) the humanpreoccupation with alien life forms; and (ii)the genesis and goals of the astrobiology fieldof science.cellular replication).Figure 2.3presentsapossible scenario of eventsleading from sterile Earththroughthe"RNA world"to cellular life.RNA-based proto-life is a likely intermediary step because RNAhas both self-replication and catalytic traits. However, proteins are superior to RNAas catalysts and DNAis superiorto RNAas a stablereservoir of genetic
32 CHAPTER 2 FORMATION OF THE BIOSPHERE: KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTS The final paragraph of the article summarized the information presented that argued for past microbial life on Mars. In examining the martian meteorite ALH84001 we have found that the following evidence is compatible with the existence of past life on Mars: (i) an igneous Mars rock (of unknown geologic context) that was penetrated by a fluid along fractures and pore spaces, which then became the sites of secondary mineral formation and possible biogenic activity; (ii) a formation age for the carbonate globules younger than the age of the igneous rock; (iii) scanning electron micrograph and transmission electron micrograph images of carbonate globules and features resembling terrestrial microorganisms, terrestrial biogenic carbonate structures, or microfossils; (iv) magnetite and iron sulfide particles that could have resulted from oxidation and reduction reactions known to be important in terrestrial microbial systems; and (v) the presence of polycyclic aromatic hydrocarbons associated with surfaces rich in carbonate globules. None of these observations is in itself conclusive for the existence of past life. Although there are alternative explanations for each of these phenomena taken individually, when they are considered collectively, particularly in view of their spatial association, we conclude that they are evidence for primitive life on early Mars. About 3 years subsequent to McKay and colleague’s publication, each of the five arguments for ancient martian microbial life was challenged in the scientific literature (e.g., Anders, 1996; Borg et al., 1999). Alternative, largely chemical, mechanisms were found for the formation of what McKay et al. had argued to be biogenic structures. Now, the general consensus is that this hypothesis about ancient martian life has been disproven. The intellectual and scientific exercise of seeking extraterrestrial life has, nonetheless, been beneficial to environmental microbiology. A new discipline has been born – astrobiology. Advances in the astrobiology scientific community have enabled it to be far better prepared to document new forms of microbial life. Research essay assignment The terms “extremophile”, “exobiology”, and “astrobiology” have been used extensively in both the scientific and nonscientific literature. After finding about six published works addressing these topics, write a 3–5 page essay that merges two aspects of astrobiology: (i) the human preoccupation with alien life forms; and (ii) the genesis and goals of the astrobiology field of science. cellular replication). Figure 2.3 presents a possible scenario of events leading from sterile Earth through the “RNA world” to cellular life. RNAbased proto-life is a likely intermediary step because RNA has both selfreplication and catalytic traits. However, proteins are superior to RNA as catalysts and DNA is superior to RNA as a stable reservoir of genetic 9781405136471_4_002.qxd 1/15/08 8:47 Page 32
33CHAPTER 2FORMATION OF THE BIOSPHERE:KEY BIOGEOCHEMICALAND EVOLUTIONARY EVENTSinformation.In the scenario shown in Figure 2.3, RNA's role in meta-bolismgraduallyshiftedtointermediarytemplatebetweeninformation-bearing DNA and substrate-specificprotein catalysts.Several of thekeystepsthoughtcrucialtolife'sdevelopmentarediscussedbelow.2.5MINERALSURFACES:THEEARLYIRON/SULFURWORLDCOULDHAVEDRIVENBIOSYNTHESISAlthoughsomeorganicchemicalscanbesynthesizedfromsimpleinor-ganic gases inthe presence of electrical discharges (see above),the openwaters of ancient seas are not the likely site of life's key early develop-mental stages. One reason for this is that water participates in hydro-lyticcleavagereactions-whicharenotconducivetobuildingcomplexorganicmolecules.In contrast,mineral surfaces[particularly ironmono-sulfide(Fes)minerals liningmicroporous rocks at thebottomof ancientseas) are currentlythought to be the site where early lifebegan (Martinand Russell, 2003).These rock formations, analogous to today's hydro-thermal vents (Figure2.4),offered three-dimensional compartmentsofUV2F0(1)+2Ht→2F(l)+H2$20'C4-10kmWastePorousmoundPH~51D6~10mhighpH andredox trontatwarmseepageOcean floorPhosphateCO,Fe(l)OceaniccrustF,Ni..H福DescendingAlkalineSearhydrothemalseawaterMembranous frothRS-solution268CO2-100°COxidationPH-10S3KmHydrationCarbonationFoNi-100°C+Fes-40CMinororganic synthesisOrganic synthesisand tractionation生乡生生生E生3H2CO CO,CHaS21mmFigure 2.4 The submarine setting for the emergence of life. (From Russell, M.J.2003Geochemistry:theimportanceofbeingalkaline.Science302:580-58l.Reprintedwithpermissionof AAAS.)
information. In the scenario shown in Figure 2.3, RNA’s role in metabolism gradually shifted to intermediary template between informationbearing DNA and substrate-specific protein catalysts. Several of the key steps thought crucial to life’s development are discussed below. 2.5 MINERAL SURFACES: THE EARLY IRON/SULFUR WORLD COULD HAVE DRIVEN BIOSYNTHESIS Although some organic chemicals can be synthesized from simple inorganic gases in the presence of electrical discharges (see above), the open waters of ancient seas are not the likely site of life’s key early developmental stages. One reason for this is that water participates in hydrolytic cleavage reactions – which are not conducive to building complex organic molecules. In contrast, mineral surfaces [particularly iron monosulfide (FeS) minerals lining microporous rocks at the bottom of ancient seas] are currently thought to be the site where early life began (Martin and Russell, 2003). These rock formations, analogous to today’s hydrothermal vents (Figure 2.4), offered three-dimensional compartments of Figure 2.4 The submarine setting for the emergence of life. (From Russell, M.J. 2003. Geochemistry: the importance of being alkaline. Science 302:580–581. Reprinted with permission of AAAS.) CHAPTER 2 FORMATION OF THE BIOSPHERE: KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTS 33 9781405136471_4_002.qxd 1/15/08 8:48 Page 33
34CHAPTER2FORMATION OF THE BIOSPHERE:KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTSdiffusion-limitedhydrophobicsurfacesthatcouldCH,-COOHCO2CH-SHbind and concentrate organic compounds.In addi-A许tion,Fes and nickel monosulfide (Nis)catalystsSCH3CHSlining the porous cavities are capable of forgingCHO=②COcarbon-carbon bonds (HuberandWachtershauser,HOCOCHS2006; see Section 7.1).The geochemical contextH,S/CoHCO,Hof these porous mineral surfaces was along gra-CO-CO-CH,Fe,Co,NiOCdients of oxidation/reductionpotential,pH,andtemperature where sulfide-rich hydrothermalClusterimineralcOfluid mixedwithFe(Il)-containing watersof thelibraryONH.ocean floor.Under such conditions oxidative for-COOHmationofpyrite(FeS)occursspontaneously:PeptideAlaCO?library?CHSFeS+H,S-→FeS,+H,△G=-38.4kJ/molFigure 2.5 Reactions in the iron/sulfurThis type of exothermic reaction produces re-world.Shownaretheproposedreactionducing power (H2),often essential in biosyn-schemes for primordial molecules at catalyticthetic reactions. It also can drive the autocatalyticsurfaces intheiron/sulfur world.Reactionassemblyof complexorganicmolecules (Figure2.5;stepslead to the conversion of carbonWachtershauser,1990,1992).Current thoughtmonoxide(l)to a varietyofkeybiomolecules,including:methyl thioacetate (2),pyruvate(MartinandRussell,2003)holdsthatthechem-(3),and alanine (4). (From Wachtershauser,istryoftheRNAworld(indludingreductionofCOG.2000. Origin of life: Life as we don't knowand COzpeptidebondformation;synthesis ofit.Science289:1307-1308.Reprinted withnucleotides;and formation of thioesterprecursorspermission of AAAs.)ofATP)occurredintheseFeScavities.2.6 ENCAPSULATION:AKEYTOCELLULARLIFEAs defined above,proto-life (organic catalysis and replication)wasconfined to the rocky pores where the RNA world began.Themobile,compartmentalizedcharacterofmoderncellshadyettobeinvented.Theactive sites of modern enzymes still rely upon Fes-and Nis-type moiet-ies; thus, it is likely that the early enzymes simply incorporated bits oftheir mineral heritage (see Section 7.1).Regarding encapsulation into mem-brane-boundcompartments,experimentsbyD.Deamerinthe197osshowed that fattyacids have the capacityto self-assemble into membranelikevesicles.More recently.Hanczyc etal.(2oo3)havedemonstrated thatconditions likelyto prevail on an ancient seafloor (catalytic surfaces, hydro-dynamicforces,alkalineconditions)havethepotentialtofosterforma-tion,growth, and division of fatty acid-based membranes that enclosebiomolecules.Thus,the rudimentarymechanisms leading from surface-catalyzedproto-lifetofree-livingcellsseemtohavebeenestablished(seeFigure 2.3)
diffusion-limited hydrophobic surfaces that could bind and concentrate organic compounds. In addition, FeS and nickel monosulfide (NiS) catalysts lining the porous cavities are capable of forging carbon–carbon bonds (Huber and Wachtershauser, 2006; see Section 7.1). The geochemical context of these porous mineral surfaces was along gradients of oxidation/reduction potential, pH, and temperature where sulfide-rich hydrothermal fluid mixed with Fe(II)-containing waters of the ocean floor. Under such conditions oxidative formation of pyrite (FeS2) occurs spontaneously: FeS + H2S → FeS2 + H2 ∆G = −38.4 kJ/mol This type of exothermic reaction produces reducing power (H2), often essential in biosynthetic reactions. It also can drive the autocatalytic assembly of complex organic molecules (Figure 2.5; Wachtershauser, 1990, 1992). Current thought (Martin and Russell, 2003) holds that the chemistry of the RNA world (including reduction of CO and CO2; peptide bond formation; synthesis of nucleotides; and formation of thioester precursors of ATP) occurred in these FeS cavities. 2.6 ENCAPSULATION: A KEY TO CELLULAR LIFE As defined above, proto-life (organic catalysis and replication) was confined to the rocky pores where the RNA world began. The mobile, compartmentalized character of modern cells had yet to be invented. The active sites of modern enzymes still rely upon FeS- and NiS-type moieties; thus, it is likely that the early enzymes simply incorporated bits of their mineral heritage (see Section 7.1). Regarding encapsulation into membrane-bound compartments, experiments by D. Deamer in the 1970s showed that fatty acids have the capacity to self-assemble into membranelike vesicles. More recently, Hanczyc et al. (2003) have demonstrated that conditions likely to prevail on an ancient seafloor (catalytic surfaces, hydrodynamic forces, alkaline conditions) have the potential to foster formation, growth, and division of fatty acid-based membranes that enclose biomolecules. Thus, the rudimentary mechanisms leading from surfacecatalyzed proto-life to free-living cells seem to have been established (see Figure 2.3). 34 CHAPTER 2 FORMATION OF THE BIOSPHERE: KEY BIOGEOCHEMICAL AND EVOLUTIONARY EVENTS Figure 2.5 Reactions in the iron/sulfur world. Shown are the proposed reaction schemes for primordial molecules at catalytic surfaces in the iron/sulfur world. Reaction steps lead to the conversion of carbon monoxide (1) to a variety of key biomolecules, including: methyl thioacetate (2), pyruvate (3), and alanine (4). (From Wachtershauser, G. 2000. Origin of life: Life as we don’t know it. Science 289:1307–1308. Reprinted with permission of AAAS.) 9781405136471_4_002.qxd 1/15/08 8:48 Page 34