Oxygen and the Evolution of Life . Heinz Decker Kensal E. van Holde l Oxygen and the Evolution of Life ProfessorDr.HeinzDecker KensalE.vanHolde Institutfu¨rMolekulareBiophysik DistinguishedProfessorEmeritus JohannesGutenberg-Universita¨tMainz DeptofBiochemistryandBiophysics JakobWelderWeg.26 OregonStateUniversity 55128Mainz,Germany CorvallisOR97331 [email protected] USA [email protected] ISBN978-3-642-13178-3 e-ISBN978-3-642-13179-0 DOI10.1007/978-3-642-13179-0 #SpringerHeidelbergDordrechtLondonNewYork #Springer-VerlagBerlinHeidelberg2011 Thisworkissubjecttocopyright.Allrightsarereserved,whetherthewholeorpartofthematerialis concerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation,broadcasting, reproductiononmicrofilmorinanyotherway,andstorageindatabanks.Duplicationofthispublication orpartsthereofispermittedonlyundertheprovisionsoftheGermanCopyrightLawofSeptember9, 1965,initscurrentversion,andpermissionforusemustalwaysbeobtainedfromSpringer.Violations areliabletoprosecutionundertheGermanCopyrightLaw. Theuseofgeneraldescriptivenames,registerednames,trademarks,etc.inthispublicationdoesnot imply, even in the absence of a specific statement, that such names are exempt from the relevant protectivelawsandregulationsandthereforefreeforgeneraluse. Cover illustration: Different oxygen transport (respiratory) proteins developed after the oxygen concentrationincreasedsomebillionyearsago:earthwormhemoglobin(red),arthropodhemocyanin (scorpion),molluschemocyanin(cephalopod)(frontcover,clockwise)andthemyriapodhemocyanin (back cover); see also Fig. 5.8. The molecules artwork are courtesy of Ju¨rgen Markl, Institute for Zoology,JohannesGutenbergUniversityMainz. Coverdesign:WMXDesignGmbH,Heidelberg,Germany Printedonacid-freepaper SpringerispartofSpringerScienceþBusinessMedia(www.springer.com) Preface This book has a curious history. It evolved, like its subject, from a much simpler beginning. Both the authors have had long-standing common interests in the proteins and processes of oxygen transport in animals. During a sabbatical year that KvH spent in the laboratory of HD, our discussions broadened to encompass the much deeper question as to how oxygen transport, and indeed oxygen utiliza- tion, were related to the evolution of life. As we considered the geological and paleontological evidence, it became clear that changes in the earth’s atmosphere andbiologicalevolutionhavebeen,andcontinuetobe,interrelatedincomplexand fascinatingways.Furthermore,theserelationshipshaveimportantimplicationsfor humanhealthandhumanity’sfuture. Thus, the book grew outward from its original focus on oxygen transport, sometimes into areas in which we must confess less confidence than we would like.But,wemustaskthereader’sindulgence,forwefeelthatthefascinationofthe wholestorysuchthatitisvitaltotrytotellit. One of us (KvH) wishes to express his thanks to the Alexander von Humboldt Foundation, whose generous support allowed the sabbatical in the Decker labora- tory. Later, both started the book at the stimulating environment of the Marine BiologicalLaboratoryatWoodsHolewhereHDspenthissabbatical. SomereadersmayfindChapter1daunting,withtoomuchdrychemistry.Skipit ifyouwish!Althoughwefeelthatitprovidesausefulbackgroundfortherestofthe book,mostofthefollowingChapterscanbereadintelligentlywithoutthismaterial. We would like to thank Dr. Helmut Ko¨nig, Dr. Wolfgang Mu¨ller-Klieser, and Dr.HaraldPaulsen(UniversityofMainz)forcriticalreadingofseveralpartsofthe bookandChristianLozanoskyforhishelpwiththefigures.WealsothankDr.Jutta Lindenborn(Springer)forallherhelpwiththepublishingprocess. We would like to express our thanks to our wives, Ina Decker and (the late) BarbaravanHoldefortheirpatienceduringthepastyears. Mainz,Germany HeinzDecker Corvallis,OR,USA KensalE.vanHolde v . Contents 1 Oxygen,ItsNatureandChemistry:WhatIssoSpecialAbout ThisElement? .............................................................. 1 1.1 ABriefIntroductiontoOxygen ....................................... 1 1.2 AtomicStructureofOxygen:ChemicalBondingPotential .......... 2 1.3 TheDioxygenMolecule ............................................... 5 1.4 ReactiveOxygenSpecies ............................................. 8 1.4.1 Superoxide1O (cid:2)* ............................................... 8 2 1.4.2 Hydrogenperoxide(H O ) ..................................... 9 2 2 1.4.3 Peroxylradical(ROO*) ......................................... 9 1.5 Ozone ................................................................. 10 1.6 Water ................................................................. 12 1.7 WaterVaporintheAtmosphere ..................................... 15 1.8 CarbonDioxide ....................................................... 15 1.9 SolubilityofGasesinWater ......................................... 16 1.10 HydrolysisandDehydration:CentralWaterReactions inBiology ........................................................... 16 1.11 RedoxReactions ...................................................... 17 References .................................................................. 18 2 ABriefHistoryofOxygen ................................................ 21 2.1 CosmicHistoryoftheElements ....................................... 21 2.1.1 TheSunandSolarSystem ...................................... 24 2.2 FormationofEarth ..................................................... 25 2.3 ThePrimordialEnvironment .......................................... 27 2.3.1 AtmosphereoftheEarlyEarth ................................. 27 2.3.2 WaterontheEarth’Surface:TheOriginofOceans ........... 29 2.3.3 TheFirstGreenhouseEffect .................................... 29 2.4 Life:ItsOriginsandEarliestDevelopment ........................... 30 2.5 ABillionYearsofLifeWithoutDioxygen:AnaerobicMetabolism ... 32 2.5.1 SomePrinciplesofMetabolism ................................ 32 2.6 TheInventionofPhotosynthesis ...................................... 35 vii viii Contents 2.7 HowOxygenicPhotosynthesisRemodeledtheEarth ................. 38 2.7.1 TheFirstRiseofDioxygen ..................................... 38 2.7.2 EffectsonLife:AnEcologicalCatastrophe? .................. 39 2.7.3 EffectsontheEarth ............................................. 40 References .................................................................. 41 3 CopingwithOxygen ...................................................... 43 3.1 TheImpactofOxygenationonanAnaerobicWorld ................. 43 3.2 ProductionofReactiveOxygenSpecies .............................. 44 3.3 CopingwithReactiveOxygenSpecies ................................ 47 3.3.1 ScavengerMolecules ........................................... 47 3.3.2 EnzymesforDetoxificationofROS ............................ 49 3.3.3 AntioxidantEnzymeSystems .................................. 51 3.4 HowtoAvoidReactiveOxygenSpecies? ............................ 52 3.5 EvolvingDefenseStrategies ........................................... 53 3.5.1 AggregationforDefense ........................................ 53 3.5.2 Melanin ......................................................... 54 3.5.3 OxygenTransportProteinsPreventCreation ofOxygenRadicals ............................................. 55 3.6 ReactiveOxygenSpeciesasCellularSignals ......................... 56 3.7 DioxygenasaSignal:OxygenSensor ................................ 56 3.8 Summary:ReactiveOxygenSpeciesandLife ........................ 57 References .................................................................. 58 4 AerobicMetabolism:BenefitsfromanOxygenatedWorld ........... 61 4.1 TheAdvantagetoBeingAerobic ..................................... 61 4.2 EvolutionofanAerobicMetabolism .................................. 62 4.2.1 SpecialMechanismsNeededforAerobicMetabolism ........ 62 4.2.2 WhenandHowDidAerobesArise? ........................... 63 4.3 Eukaryotes:TheNextStepinEvolution .............................. 67 4.3.1 DistinctionBetweenProkaryotesandEukaryotes ............. 67 4.3.2 TheSymbioticHypothesis ...................................... 67 4.4 TheLastGreatLeap:MulticellularOrganisms,“Metazoans” ........ 69 4.4.1 When,Why,andHow? ......................................... 69 4.4.2 CollagenandCholesterin ....................................... 70 4.4.3 HalfaBillionYearsofStasis? ................................. 71 4.4.4 EmergenceandExtinctionoftheEdiacaranFauna ............ 72 4.4.5 TheBilateralBodyPlan ........................................ 73 4.4.6 The“CambrianExplosion”:FactorArtifact? ................. 74 References .................................................................. 76 5 FacilitatedOxygenTransport ............................................ 79 5.1 HowtoDeliverDioxygentoAnimalTissues? ...................... 79 5.2 ModesofDelivery .................................................... 80 Contents ix 5.2.1 DiffusionfromtheSurface .................................... 80 5.2.2 TransportviaBloodasaDissolvedGas ...................... 81 5.2.3 OxygenTransportProteins:WhatTheyMustDo? ........... 82 5.3 ModesofDioxygenBindingtoOxygenTransportProteins ........ 84 5.3.1 CooperativeandNoncooperativeBinding .................... 84 5.3.2 HowDoesCooperativityWork?:ModelsforAllostery ...... 86 5.3.3 Self-AssemblyandNesting .................................... 88 5.3.4 WhyComplexMultisubunitOxygenTransportProteins? .... 89 5.4 ModulationofDioxygenDeliverybyOxygenTransportProteins: Heteroallostery ....................................................... 89 5.4.1 ModulationbytheProductsofAnaerobicMetabolism: theBohrEffect ................................................. 90 5.4.2 TheHaldaneEffect ............................................ 90 5.4.3 TheRootEffect ................................................ 91 5.4.4 TemperatureDependence ...................................... 92 5.4.5 EvolutionaryAspectsofRegulation ........................... 93 5.5 DiversityofOxygenTransportProteins ............................. 93 5.5.1 Hemoglobins ................................................... 94 5.5.2 Hemerythrins ................................................... 96 5.5.3 Hemocyanins ................................................... 96 5.6 EvolutionofOxygenTransportProteins ............................. 99 5.7 WasSnowballEarthaPossibleTriggerforOPTEvolution? ...... 101 5.8 FromWhatProteinsDidOxygenTransportProteinsEvolve? ..... 102 5.9 OxygenTransportProteinsand“IntelligentDesign” ............... 103 References ................................................................. 103 6 ClimateOvertheAges;IstheEnvironmentStable? .................. 107 6.1 ClimateandGlaciationsinEarth’sHistory .......................... 108 6.1.1 TheFirstMassiveGlaciations;theHuronionEvent:ARole forMethane? ................................................... 108 6.1.2 LaterProterozoicGlaciations .................................. 110 6.1.3 PhanerozoicClimateandGlaciations ......................... 111 6.2 HowDidLifeSurviveGlaciations? .................................. 116 6.3 MilestonesofLifeinthePhanerozoic ................................ 118 6.4 InorganicCyclingofCarbonDioxide ................................ 121 6.5 IsOurEnvironmentStable? .......................................... 122 6.6 RecentGlobalWarming .............................................. 124 References ................................................................. 124 7 GlobalWarming:HumanInterventioninWorldClimate ........... 127 7.1 RecentClimateChanges .............................................. 127 7.2 PhysicalConsequencesofGlobalWarming ......................... 129 7.2.1 ShrinkingIceandGlaciers .................................... 129 7.2.2 SeaLevelChanges ............................................. 130 7.2.3 ChangesinOceanCurrents .................................... 131 x Contents 7.2.4 LocalClimateandWeather ................................... 132 7.2.5 TheDangerofMethaneReleases ............................. 133 7.2.6 GreenhousetoIcehouseandViceVersa? ..................... 133 7.3 HumanConsequencesofGlobalWarming ........................... 134 7.3.1 DirectConsequencesofCO andTemperatureIncrease ..... 134 2 7.3.2 SeaLevelRise ................................................. 135 7.3.3 ExtremeWeather .............................................. 136 7.3.4 EffectsonAgriculture ......................................... 137 7.4 ControlofGlobalWarming .......................................... 138 7.4.1 PositiveandNegativeNaturalFeedbackMechanism ......... 138 7.4.2 HumanEffectstoControlGlobalWarming .................. 139 7.4.3 TheLongView ................................................ 139 References ................................................................. 140 8 OxygeninMedicine ...................................................... 143 8.1 Hypoxia ............................................................... 143 8.1.1 High-AltitudeHypoxia ........................................ 144 8.1.2 HypoxiaArisingfromMedicalConditions ................... 145 8.2 OxidativeStress ....................................................... 145 8.2.1 NatureofOxidativeStress ..................................... 145 8.2.2 SpecialExamplesofMedicalConsequences ofOxidativeStress ............................................. 146 8.3 TreatmentofOxidativeStress ........................................ 149 8.4 BeneficialRolesofROS .............................................. 150 8.4.1 SCNandPrimaryImmuneResponse ......................... 150 8.4.2 NitricOxide .................................................... 151 References ................................................................. 153 9 OxygenandtheExplorationoftheUniverse .......................... 157 9.1 WhatIsEssentialfortheDevelopmentofLifeasWeKnowIt? .... 157 9.2 WhatMakesO NecessaryforComplexLifeonHabitable 2 Planets? ............................................................... 158 9.3 SeekingEvidenceforExtraterrestrialLife ........................... 158 9.4 LifeintheSolarSystem? ............................................. 161 9.4.1 TerrestrialPlanets .............................................. 161 9.4.2 IcyMoons ...................................................... 163 9.5 OxygenSupplyProblemsinExtraterrestrialVoyages ............... 164 9.6 ProblemsFacingExtendedExtraterrestrialSettlement orColonizaton ........................................................ 166 9.6.1 AdjustingthePlanetaryEnvironment:Terraforming ......... 166 9.6.2 AdjustingtheOrganism:Bioforming ......................... 167 References ................................................................. 168 Index .......................................................................... 169