FMT150光养生物反应器文献—2012 ELEVATED CARBON DIOXIDE DIFFERENTIALLY ALTERS THE PHOTOPHYSIOLOGY

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ELEVATEDCARBONDIOXIDEDIFFERENTIALLYALTERSTHEPHOTOPHYSIOLOGYOFTHALASSIOSIRAPSEUDONANA(BACILLARIOPHYCEAE)ANDEMILIANIAHUXLEYI(HAPTOPHYTA)1

AveryMcCarthy2,SusanP.Rogers,StephenJ.Duffy,andDouglasA.Campbell3DepartmentofChemistry&Biochemistry,MountAllisonUniversity,Sackville,NewBrunswick,E4L1G7,Canada

Increasinganthropogeniccarbondioxideiscaus-ingchangestooceanchemistry,whichwillcontinueinapredictablemanner.Dissolutionofadditionalatmosphericcarbondioxideleadstoincreasedcon-centrationsofdissolvedcarbondioxideandbicar-bonateanddecreasedpHinoceanwater.Theconcomitanteffectsonphytoplanktonecophysiol-ogy,leadingpotentiallytochangesincommunitystructure,arenowafocusofconcern.Therefore,wegrewthecoccolithophoreEmilianiahuxleyi(Loh-mann)W.W.HayetH.MohlerandthediatomstrainsThalassiosirapseudonana(Hust.)HasleetHeimdalCCMP1014andT.pseudonanaCCMP1335underlowlightinturbidostatphotobioreactorsbubbledwithaircontaining390ppmvor750ppmvCO2.IncreasedpCO2ledtoincreasedgrowthratesinallthreestrains.Inaddition,proteinlevelsofRUBISCOincreasedinthecoastalstrainsofbothspecies,showingalargercapacityforCO2assimila-tionat750ppmvCO2.WithincreasedpCO2,bothT.pseudonanastrainsdisplayedanincreasedsuscep-tibilitytoPSIIphotoinactivationand,tocompen-sate,anaugmentedcapacityforPSIIrepair.Consequently,thecostofmaintainingPSIIfunctionforthediatomsincreasedatincreasedpCO2.InE.huxleyi,PSIIphotoinactivationandthecounter-actingrepair,whilebothintrinsicallylargerthaninT.pseudonana,didnotchangebetweenthecurrentandhigh-pCO2treatments.Thecontentofthepho-tosyntheticelectrontransportintermediarycyto-chromeb6⁄fcomplexincreasedsignificantlyinthediatomsunderelevatedpCO2,suggestingchangesinelectrontransportfunction.Keyindexwords:cytochromeb6f;electrontrans-port;Emilianiahuxleyi;growthrate;oceanacidifi-cation;pCO2;pH;photoinhibition;RUBISCO;ThalassiosirapseudonanaAbbreviations:CCMs,carbonconcentratingmecha-nisms;CCMP,Provasoli-GuillardNationalCenterfortheCultureofMarinePhytoplankton;CO2(aq),dissolvedCO2;DCMU,3-(3,4-dichlorophenyl)-1,1-dimethylurea;DIC,dissolvedinorganiccar-bon;EASW,enrichedartificialseawater;ETR,electrontransportrate;FIRe,fluorescenceinduc-tionandrelaxation;FMDARK,maximumfluores-

cenceinthedark-adaptedstate;FMDCMU,maximalfluorescenceinthepresenceofDCMU;FM¢,

maximumfluorescenceinthelight-adaptedstate;FO,minimumfluorescenceinthedark-adaptedstate;FO¢,minimumfluorescenceinthelight-adaptedstate;FS,steady-statefluorescenceinthelight-adaptedstate;FV,variablefluorescence;KM,

half-saturationconstant;NPQ,nonphotochemical

quenching;pCO2,partialpressureofCO2;qL,

photochemicalquenching;RPSII,PSIIrepairrate;

TA,totalalkalinity;rI,effectiveabsorptioncrosssectionforphotonsdrivingPSIIphotoinactiva-tion;rPSII,thefunctionalabsorptioncrosssection

servingPSIIphotochemistry;Xcalcite,calcitesaturationstate

Forthepast10millionyears,theatmosphericpartialpressureofCO2(pCO2)remainedbelow300

ppmv(Berner1990,PearsonandPalmer2000),butsincetheIndustrialRevolutionanthropogenicCO2

hasraisedpCO2to390ppmv,andpCO2ispro-

jectedtoreach$750ppmvbytheyear2100(Houghtonetal.2001).TheatmosphereandthesurfaceoceanexchangeCO2ontimescalesofsev-

eralmonths(ZeebeandWolf-Gladrow2001),soincreasesinatmosphericpCO2leadtoincreasesinoceanicdissolvedCO2(CO2(aq)),bicarbonate,and

hydrogenionconcentrations,butdecreasesincar-bonateionconcentrations(CaldeiraandWickett2005).Furthermore,theconcentrationsandbioavai-labilitiesofammonia,ammonium,iron,phosphate,silicate,andtoxinswillbeaffectedthroughpH-dependentspeciationandsolubility(ZeebeandWolf-Gladrow2001).Althoughthesepredictedchangesinseawaterchemistryarewelldescribed,theeffectsonmarineorganismsandecosystemsarenotasclear.Theresponsesofphytoplanktontochangingseawaterchemistrymayvaryamongtaxa,

1Received4July2011.Accepted8December2011.

2Presentaddress:DepartmentofBiology,Biological&Geological

SciencesBuilding,UniversityofWesternOntario,London,Ontario,CanadaN6A5B7.3Authorforcorrespondence:e-maildcampbell@mta.ca.

J.Phycol.48,635–646(2012)Ó2012PhycologicalSocietyofAmerica

DOI:10.1111/j.1529-8817.2012.01171.x

635whichhavedivergentnutrientuptakesandmeta-

bolicresourceallocations(Quiggetal.2003).Diatomsareresponsiblefor$40%ofcurrentmarineprimaryproductivity(Fieldetal.1998)andtendtodominatethephytoplanktonassemblageundernutrient-richconditions,especiallyinturbu-lentcoastalwaterswithfluctuatinglight(Macintyreetal.2000),inpartbecausetheyshowlowsuscepti-bilitytophotoinactivationcomparedtootherphyto-plankton(Keyetal.2010,Loebletal.2010).Incomparisontootherphytoplankton,diatomshaveahighefficiencyofcarbonsequestrationintothedeepoceanastheirheavysilicafrustulesenhancesinkingrates(Smetacek1999).TheyhaveaformIDRUBISCOwithgreaterCO2⁄O2selectivity,butalowerhalf-saturationconstant(KM)thanmanyotheralgae(Badgeretal.1998,Tcherkezetal.2006).BothcurrentandpredictedfutureseawaterCO2(aq)concentrationsarewellbelowthelevelsrequiredtosaturatetheirisolatedRUBISCOenzyme(RostandRiebesell2004).However,manydiatoms,especiallybloom-formingones,haveactivecarbonconcentrat-ingmechanisms(CCMs)(Burkhardtetal.2001)toaccumulatebothCO2andbicarbonateforphotosyn-thesis(Satohetal.2001,Colmanetal.2002,Moreletal.2002,Badger2003).AsCO2(aq)andbicarbon-ateconcentrationsrise,diatomscouldderivenetbenefitsthroughdown-regulationoftheirCCMs,freeingresourcesforotherbiologicalprocesses.InthediatomPhaeodactylumtricornutumgrowthisindeedstimulatedatthepredictedfutureCO2con-centrationof750ppmv(Wuetal.2010).Further-more,increasedCO2concentrationscausedshiftsinthedominanceofdiatomspeciesinthephytoplank-tonassemblageoftheEquatorialPacific(Tortelletal.2002),andoftheSouthernOcean(Tortelletal.2008).Coccolithophoresareanothergroupofgloballydistributedphytoplanktonwhichformextensivebloomsinthecurrentocean.Thecoccolithophoresaremajorcalcifiersintheoceanbecausetheypro-ducecalciumcarbonatescalestermedcoccoliths,whichcoverthecell(Baumannetal.2004).Cocco-lithophoreshavebeenafocusforstudiesonphyto-planktonresponsestoincreasedpCO2,astheircalcificationshowssensitivitytopH(Riebeselletal.2000).Predicteddropsinseawatercarbonatecon-centrationswilldecreaseinthesaturationstatesofaragoniteandcalcite(Xcalcite),whichcouldnega-tivelyaffectcalcificationincoccolithophores(Morseetal.2007).InearlystudiesthecoccolithophoresEmilianiahuxleyiandGephyrocapsaoceanicadisplayeddecreasedcalcificationrateswithincreasingpCO2(Riebeselletal.2000,Zondervanetal.2001).Thisdropincalcificationratewashypothesizedtodecreasetheircompetitiveness.SimilarresponsesofdecreasedcalcificationunderelevatedpCO2wereshowninanumberofsubsequentstudiesbothincultures(Zondervanetal.2001,Sciandraetal.2003),andinmesocosms(Delilleetal.2005,Engeletal.2005).Anotherstudy,however,showedtheoppositetrendwithcalcificationinE.huxleyiincreasingunderthefutureocean,elevatedpCO2scenario(Iglesias-Rodriguezetal.2008).Calcifica-tionintwolarger,heavilycalcifyingcoccolithophorespecies(Langeretal.2006)showedanoptimumcurvewithCO2(C.leptoporus)butinsensitivitytoCO2inC.pelagicus.CoccolithophorespossessaformIDRUBISCOandthecellshaveHCO3-channels(Herfortetal.2002).Nevertheless,currentCO2(aq)concentrationsarenotsaturatingforphotosynthesisinE.huxleyi(RostandRiebesell2004),whichcouldthusbenefitfromgreaterCO2(aq)concentrations.ThesensitivityofphytoplanktontovariablelightcouldalsochangeunderincreasedpCO2.Photoin-