Ordered low-temperature dolomite mediated by carboxyl-group density microbial cell walls - 图文

Orderedlow-temperaturedolomitemediatedbycarboxyl-groupdensityofmicrobialcellwalls

PaulA.Kenward,DavidA.Fowle,RobertH.Goldstein,

MasatoUeshima,LuisA.González,andJenniferA.Roberts

ABSTRACT

Abundantintheancientrockrecord,earlydolomiteremainsscarceinmodernsystemsatlowtemperatures(<50°C),eventhosesystemssupersaturatedwithrespecttodolomite.ThisscarcityisattributedtokineticinhibitionincludingcomplexationofMg2+bywaterandsulfate,carbonateactivity,andMg:Caratio.Recentinvestigationspointtoafunctionformicrobialmetabolismsandsurfaces,inwhichdisorderedphasesareformed.Here,wereporttheprecipitationofprimaryor-dereddolomiteat30°C,facilitatedsolelybythecellwallsoftwononmetabolizingarchaeafromsalinesolutionswithanMg:Caratioof1:1,5:1,and10:1,andslightlysaturatedwithrespecttodolomite.Controlexperimentsusingbacteriaandfunctionalizedmicrospheresdidnotprecipitatedolomite.Archaealcellwallfunctionalgroupswereapproximatelyoneorderofmagnitudehigherthanthebacteriaandspheresusedinthisstudy.Fromtheseresults,weproposeamechanisticmodelinwhichcarboxylgroupsassociatedwithcellwallbiomassandexopolymericsubstancesdehydrateMgions,furtherpromotingcar-bonationandleadingtodolomitenucleation.Thesedataexplainre-portsoflow-temperaturedolomiteformationassociatedwithnumer-ousmicrobialmetabolicguilds,includingbacteriaandarchaea,andthosereportedinassociationwithexopolymericsubstancesorcellwallsurfaces,andidentifyakeyandwidespreadmechanismintheforma-tionofdisordereddolomiteandorderedprimaryphasesofdolomiteatlowtemperature.Importantly,thefunctionalizeddeadandnon-metabolizingbiomassisthekeyinlow-temperaturedolomitepre-cipitation,notactivemicrobialmetabolism.Theseobservationsmayleadtonewpredictivemodelsforthedistributionofdolomite.

INTRODUCTION

Primarydolomiteformationatlowtemperaturesiskineticallyinhibitedatlowtemperatures(McKenzie,1991;Land,1998).Slowreaction

Copyright?2013.TheAmericanAssociationofPetroleumGeologists.Allrightsreserved.

ManuscriptreceivedOctober10,2012;provisionalacceptanceMarch14,2013;revisedmanuscriptreceivedApril24,2013;finalacceptanceMay17,2013.DOI:10.1306/05171312168

AAPGBulletin,v.97,no.11(November2013),pp.2113–21252113

AUTHORS

PaulpartmentA.KenwardofGeology,$MultidisciplinaryUniversityofKansas,ResearchDe-Building,2030BeckerDrive,Lawrence,Kansas;thepkone@gmail.com

PaulA.KenwardreceivedhisB.S.degreefromtheUniversityofOttawa,Ottawa,Ontario,Canada(2002),hisM.S.degreefromtheUniversityofWindsor,Windsor,Ontario,Canada(2005),andhisPh.D.fromtheUniversityofKansas(2010).Hestudiesmicrobialinfluencesoncarbonatemineralprecipitation.

DavidpartmentA.ofFowleGeology,$MultidisciplinaryUniversityofKansas,ResearchDe-Building,2030BeckerDrive,Lawrence,Kansas;fowle@ku.edu

DavidA.FowleisanassociateprofessorattheUniversityofKansas.HereceivedhisB.Sc.degreefromWesternUniversity,inLondon,Ontario,Canada,andhisM.S.degreeandPh.D.fromtheUniversityofNotreDame.Hisresearchfocusesonstudyingthefunctionofmicrobiallymediatedprocessesonbiogeochemicalcycles.

Robertsas,DepartmentH.GoldsteinofGeology,$University1475JayhawkofKan-Boulevard,120LindleyHall,Lawrence,Kansas;gold@ku.edu

RobertH.GoldsteinistheHaasDistinguishedProfessorattheUniversityofKansas.HereceivedhisB.S.degreefromJuniataCollege,Huntingdon,Pennsylvania,andhisM.S.degreeandPh.D.fromtheUniversityofWisconsin.Hiscurrentresearchincludesthedevelopmentofthefluid-inclusiontoolfordiageneticresearch,theintegrationofdia-genesiswithsequencestratigraphyandtectonicsetting,andtheevaluationofcontrolsonthesequence-stratigraphiccharacterofcarbonaterocks.

MasatoUeshima$UniversityofKansas,De-partmentofGeology,MultidisciplinaryResearchBuilding,2030BeckerDrive,Lawrence,Kansas;mueshima@ku.edu

MasatoUeshimaisaresearchassociateattheUniversityofKansas.HereceivedhisB.S.andM.S.degreesfromGakushuinUniversity,Tokyo,Japan,andhisPh.D.fromKanazawaUniversity,Japan.Hiscurrentresearchuseselectronmicroscopy,ana-lyticalchemistrytoinvestigateinteractionsamongmicrobes,andmineralsandsolutionsapplyingforwastedisposal.

LuisA.González$UniversityofKansas,De-partmentofGeology,MultidisciplinaryResearchBuilding,2030BeckerDrive,Lawrence,Kansas;lgonzlez@ku.edu

LuisA.GonzálezisaprofessorattheUniversityofKansasandthechairpersonoftheDepartmentofGeology.HereceivedhisB.S.degreefromtheUniversityofPuertoRico,Mayagüez,PuertoRico,andhisM.S.degreeandPh.D.fromtheUniversityofMichigan.Hiscurrentresearchusestheisotopiccomposition,mineralogy,growthhistory,andgrowthpatternsofspeleothemstoextractpaleo-climaticandpaleoenvironmentalsignals.JenniferA.Roberts$UniversityofKansas,DepartmentofGeology,MultidisciplinaryRe-searchBuilding,2030BeckerDrive,Lawrence,Kansas;jenrob@ku.edu

JenniferA.RobertsisanassociateprofessorattheUniversityofKansas.ShereceivedherB.S.degreefromTrinityUniversity,SanAntonio,Texas,andherPh.D.fromtheUniversityofTexasatAustin.Herresearchinvestigatesmicrobe-mineralinteractionsandtheirinfluenceonearlydiageneticprocesses.

ACKNOWLEDGEMENTS

WethanktheKansasUniversity(KU)GeologyAssociatesandShellInternationalExplorationandProductionforfunding,aswellasBradPratherforhiscontinuedsupportandcontributionstothisresearch.WealsothankDavidMooreandtheKUMicroscopyandAnalyticalImagingLaboratoryfortheirhelpwithimaging.FurtherfundingwasprovidedbythesupportersoftheKansasInter-disciplinaryCarbonatesConsortium(Conoco-Phillips,BHPBilliton,Devon,Shell,Chevron,Chesapeake,Pioneer,Repsol,Sandridge,SaudiAramco,andApache).

TheAAPGEditorthanksthefollowingreviewersfortheirworkonthispaper:HenryChafetzandDouglasW.Haywick.

kineticsareattributedtolowMg:Caratio,ioncomplexation,hy-drationspheres,andtheformationofneutralcomplexeswithsulfate(GoldsmithandGraf,1958;Kitano,1962;Folk,1974;FolkandLand,1975;KatzandMatthews,1977;BakerandKastner,1981;Land,1985;GonzálezandLohmann,1985;Hardie,1987;Sibleyetal.,1987;ZhongandMucci,1989;SlaughterandHill,1991;ArvidsonandMackenzie,1997;WrightandWacey,2004).Recentstudieshaveascertainedthatmicroorganismsplayafundamentalfunctioninlow-temperaturedolomiteformationinspecificenvironments,wheremicrobespresumablyaltersolutionchemistryorprovidenucleationsurfacesthatfacilitatereactionprogress(Vasconcelosetal.,1995).

Microbialdolomitehasbeenidentifiedinbothfieldandlaboratorysettings,mostcommonlyasdisordered(e.g.,protodolomite;Moreiraetal.,2004)andorderedphases(Robertsetal.,2004;Kenwardetal.,2009).Previousstudieshavetargetedthemetabolicactivityofsul-fatereducingbacteria(SRB)(VasconcelosandMcKenzie,1997;Warthmannetal.,2000;vanLithetal.,2003;WrightandWacey,2005),sulfideoxidizers(Moreiraetal.,2004),moderatelyhalophilicaerobicheterotrophs(Sánchez-Románetal.,2008),andmethanogens(Robertsetal.,2004;Kenwardetal.,2009).Allofthesephysiologictypesaltersolutionchemistrytopromotethesupersaturationofdo-lomite,andincasesoflaboratoryexperimentation,microbialactivitywasrequiredtoprecipitatedolomite.Alternatively,Zhangetal.(2012)foundthatdissolvedpolysaccharides,likethoseproducedduringorganicmatterdegradation,sorbtoCa-MgcarbonatesurfacesandpotentiallyweakenMg2+-waterbondsthatinhibitcarbonation,therebyfacilitatingtheformationofdisordereddolomite.

Manymicrobialstudiesobserveddolomiteassociateddirectlywithcellwallsorexopolymericsubstances(EPS)(Robertsetal.,2004;Vasconcelosetal.,2006;Sánchez-Románetal.,2008;Kenwardetal.,2009).AlthoughEPSandbiofilmsmaycreatemicroenvironmentsinwhichsolutionsareconcentrated(e.g.,Duprazetal.,2009),microbialsurfacesarecharged,possessingnumerousfunctionalgroupsin-cludingphosphoryl,hydroxyl,andcarboxylgroups(Fortinetal.,1997;DouglasandBeveridge,1998;Daughneyetal.,2001).Asso-ciationofmetalswiththesefunctionalgroupshasbeendemonstratedasaninitialstepinthenucleationofsomebiogenicminerals(Chanetal.,2004).Forexample,Krauseetal.(2012)foundthatMg-richdolomiteformedinEPSduringsulfatereductioninseawateranddemonstrated,usingCaisotopes,thattheinitialstepindolomitenucleationwasCa2+sorptiontoEPS.

Here,weinvestigatedtheeffectofdifferentarchaeal(Methano-bacteriumformicicumandHaloferaxsulfurifontis)andbacterial(BacillussubtilisandShewanellaputrefaciens)cellsurfacesinprecipitatingor-dereddolomiteasafunctionofMg:Caratioandthepresenceofsulfateinslightlysupersaturatedsalinesolutionsat30°Cusingrep-licatebatchreactors.Numeroussurfaces,includingextractedcellwalls,intactmetabolizingcells,intactnonmetabolizingcells,andfunctionalizedpolystyrenesphereswereusedtoisolateprobablemechanismsinsurface-mediateddolomiteprecipitation.

2114Low-TemperatureDolomiteMediatedbyMicrobialCellWallCharacter

Table1.GeochemistryandPrecipitationResultsofExperimentalDolomiteReactorsReactor

Dolomite-FormingTreatments

Methanobacteriumformicicum(cellwalls)M.formicicum(nonmetabolizing)Haloferaxsulfurifontis(cellwalls)H.sulfurifontis(nonmetabolizing)

Non–Dolomite-FormingTreatments

H.sulfurifontis,M.formicicum(metabolizing)M.formicicum(cellwalls)H.sulfurifontis(cellwalls)

M.formicicum(nonmetabolizing)

Microspheres(R-COO–),ShewanellaputrefaciensandBacillussubtilisAbiotic

Wdolomite*3.4–4.73.4–4.73.7–3.93.7–3.9

Mg:CaRatio5:110:15:1and10:11:1,5:1,and10:1

7.47.47.27.2pH**

SO42–(mM)

0000

IonicStrength0.660.660.990.99

3.4–4.73.4–4.73.7–3.93.4–4.73.4–4.73.4–4.7

1:11:1and10:1

1:11:1and5:1NoneNone

7.4/8.1;7.27.47.27.47.27.2

00000and28and28and28and28and280.66and0.990.660.990.66

0.66and0.990.66and0.99

0and28

*W=ionactivityproductKsp–1.

**Thegeochemistryofeachsystem,includingthepHlevelandtheionicstrength,remainedconstantduringthe6-weekintervals,exceptforthemetabolizingMethanobacteriumformicicuminwhichthepHlevelincreasedto8.1.

METHODS

Wechosetocontrasttwodifferentarchaeaandtwodif-ferentbacteria,allpossessingdifferentmetabolicactiv-itiesandcellwallcompositions.Duplicatebatchreactorswerecreatedusingsealed60-mLserumvialscontain-ingmetabolizingcells,cellwalls,intactnonmetabolizingcellsorfunctionalizedpolystyrenemicrospheres(1.1-mmdiameter;BangsLaboratories,Inc.),andsalinefluidswithavaryingMg:Caratioandsulfateconcentration.SolutionChemistry

SolutionswithmarinecompositionswerecomposedfromdistilledwaterandNaCl,Na2CO3,MgCl2,andCaCl2(seeTable1forsolutioncompositions)withthreedifferentMg:Caratios:10:1,5:1,and1:1.Replicateex-perimentswerecreatedwithidenticalgeochemistryasthoseinTable1,butwiththeadditionof0.028MofNa2SO4,totesttheeffectsofmarineconcentrationsofsulfateondolomiteformation.ThefinalsolutionsweresettoapHof7.2to7.4toobtainWdolomite[saturationstate=IAP/Ksp(ionactivityproduct/equilibriumcon-stantforthesolubilityproductofdolomite)]rangingfrom3.4to4.7(calculatedusingGeochemistsWorkbench;BethkeandYeakel,2009;Table1).ArangeofWdolomiteresultedwhenothercarbonatespecieswerekeptunder-saturatedunderdiversegeochemicalconditions.Allre-actorsremainedundersaturatedwithrespecttocalcite,

aragonite,siderite,andmagnesite.Ionicstrengthwassetto0.66molkg–1forallexperimentalsystems,exceptforthosewithH.sulfurifontis,torepresentsystemsclosertomarineconditions(~0.7molkg–1).Reactorscontain-ingH.sulfurifontishadametahalineionicstrengthof0.99molkg–1tomaintaincellintegrity.

MicrobialGrowthConditionsandExperimentalTreatments

Batchexperimentalreactorscontainedeitherasinglestrainarchaea(M.formicicum[ATCC{Americancul-turetypecollection}33274]orH.sulfurifontis[ATCCBAA897]),asinglestrainbacterium(B.subtilisorS.putrefaciens),orpolystyrenemicrospherescoatedwithcarboxyl,R-COO?functionalgroupsataconcentrationof105cells(spheres)mL–1.Microbialculturesweregrowntostationaryphaseunderthefollowingconditions.S.putrefaciensandB.subtiliswereculturedaerobicallyintrypticasesoybrothwith0.5%yeastat37°Cinashakerincubator(Liuetal.,2001;MatiasandBeveridge,2005).M.formicicumwasculturedinananaerobicin-cubator,usingMethanobacteriamedium(ATCCmedium1045)at30°Cunderan80%H2,20%CO2atmosphere.H.sulfurifontiswasculturedaerobicallyat37°Cinahalophilicgrowthmedium(ATCCmedium2448).Ar-chaealandbacterialcellswereharvestedfromthesta-tionaryphaseandwashedbymeansofcentrifugationandrinsedfivetimeswitha0.66-Mor0.99-MNaClsolution,

Kenwardetal.

2115

dependingonthedesiredionicstrength.Afterward,themicrobialculturesunderwentoneofthreepreparationsbeforebeinginjectedintotheprepareddolomitereac-tors:metabolizing,cellswalls,orintactnonmetabolizing.Formetabolizingreactors,concentratedcellswereaddedtodolomitereactorsuntreated.CellwallswereextractedbypassingcentrifugedculturesthroughaFrenchpress(GarenandEchols,1962)threetimes,leavingonlycellwalls.Forintactnonmetabolizingcells,theadditionofapowerfulmitochondrialuncouplingagent,carbonylcya-nidem-chlorophenylhydrazone,renderedcellsmetabol-icallyinactivebutintact(Heytler,1980).Metabolizingandintactnonmetabolizingcellswereinjectedintotheirseparatereactorstoafinalconcentrationof105cellsml?1.Cellwallfragmentswerederivedfromlysedcellsofthesameconcentrationoflivecells.Functionalizedpoly-styrenemicrospheres,usedasproxiesforchargedcellsurfaces,wereaddedtoreactorsunderthesameso-lutionconditionsasexperimentscontainingmicrobialmaterial(includingionicstrength,temperature,thead-ditionofcarbonylcyanidem-chlorophenylhydrazone,anddolomitesaturation),withtheexclusionofthecellwallfragmenttreatment.Additionally,reactorswerecreatedforthesamegeochemicalconditionslistedabovewithouttheadditionofcells,cellwallfragments,ormicrospheres.

Batchreactorscontainingcells(metabolizingandnonmetabolizing)orcellwallfragmentsofM.formicicumweresacrificedevery7daysfora42-dayperiodat30°Ctomonitorchangesinthegeochemistryleadingtotheformationofdolomite.Becausedolomitewasonlyfoundinreactorsthatequilibratedforthefull6-weekperiod,allothertreatmentsdescribedwereequilibratedfor6weeks(42days)at30°Cpriortobeingsacrificed.Geochemistry,Mineralogy,andImaging

After6weeks,reactorswereopenedunderanaerobicconditionstoobtainprecipitatedphases.A30-mLvolumeoffluidwasfilteredthrough0.2-mMfilters,whichwasairdriedintheanaerobicchamberandwasthenmountedandanalyzedusingx-raypowderdif-fractiononaBrukerAXSD8Advancex-raydiffrac-tometerwithCu-Kabeam.Thefilteredsolutionswereretainedforcation,alkalinity,andpHmeasurements.Cationsweremeasuredonanacidified(100-mLof10%ultrapureHNO3toapHlevelbelow3)sampleusingaPerkinElmerOptima5300DVinductivelycoupledplasma-opticalemissionspectrometer,whichhasananalyticalerrorof5%.Alkalinitywasdeterminedusing2116

manualtitrationtoapHlevelof3andendpointdeter-minationonanunacidifiedsample.ThepHlevelwasmeasuredimmediatelyafterfiltration.Speciationofso-lutionsandcalculationofmineralsaturationstateswereaccomplishedusingGeochemistsWorkbench8.0(BethkeandYeakel,2009).A5-mLvolumeofunfilteredsolu-tionwastreatedwith2%gluteraldehydetopreservesamplesfortransmissionelectronmicroscopy(TEM).SampleswerecharacterizedwithTEMonwhole-mountgridstovisualizeandidentifydolomiteprecipitatesandtheirassociationwithcellsurfaces.Preservedfragmentsandanyassociatedprecipitateswerewashedtwicewithultrapurewaterandcentrifugedat17,000×g,20°Cfor30min.Aftercentrifugation,thepelletsweredirectlydepositedonFormvar-coated200-squaremeshCugrids.Excesswaterwasremovedbymeansofsterilefilterpa-per,andthegridswerethenallowedtoairdryinafumehoodfor1hr.

Transmissionelectronmicroscopyobservationswereoperatedata200-kVacceleratingvoltageusingaTECNAIX-TwinG2transmissionelectronmicroscopeequippedwithadouble-tiltstage.Selected-areaelectrondiffractionwasconductedtounderstandthecrystal-lographyofmineralsattachedtothesurfaces.ElementalanalyseswereperformedwithanEDAXFEITecnaiF20X-Twinfieldemissiontransmissionelectronmicro-scopeequippedwithanenergydispersivex-raydetector(operatedat200kV)usingscanningTEMmodewithaspotsizeof300nm.

CharacterizationofArchaealCellWalls

Deprotonationconstantsandsurfacesiteconcentrationsofcellsurfacesweredeterminedfromacid-basetitra-tionsconductedunderaN2atmosphereat298K(e.g.,Feinetal.,2001)onsuspensionsofM.formicicuminabackgroundelectrolyteof0.01-MNaCltobufferionicstrength.ThesitedensityofcarboxylfunctionalgroupswasdeterminedbyanalyzingthedatausingPROTOFIT2.1software(TurnerandFein2006).CarboxylgroupsiteconcentrationsforB.subtilis(Daughneyetal.,2001),S.putrefaciens(Sokolovetal.,2001),H.sulfurifontis(Kinnebrew,2012),andEPS(Desulfovibriosp.)(Braissantetal.,2007;Bakeretal.,2010)weretakenfromtheliterature.Carboxylgroupsiteconcentrationsonthefunctionalizedpolystyrenemicrospheresare1.40×10–4molg–1(BangsLaboratories,Inc.).Carboxylgroupdensitieswerecalculatedfromconcentrationsusingav-eragedsurfaceareasfromtheliterature(vanderWaletal.,1997).

Low-TemperatureDolomiteMediatedbyMicrobialCellWallCharacter