Effects of Soluble Cadmium Salts Versus CdSe Quantum Dots on the Growth of Planktonic Pseudomonas...

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Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonicPseudomonas aeruginosa

by Patricia A. Holden

more

EffectsofSolubleCadmiumSalts

VersusCdSeQuantumDotsonthe

GrowthofPlanktonic

Pseudomonasaeruginosa

JOHN H. PRIESTER,

PETER K. STOIMENOV,

RANDALL E. MIELKE,

SAMUEL M. WEBB, |

CHRISTOPHER EHRHARDT,

JI N PING ZHANG, # GALEN D. STUCKY,

AND PATRICIA A. HOLDEN* ,

DonaldBrenSchoolofEnvironmentalScience&Management,DepartmentofChemistryandBiochemistry,EarthSciences,andMaterialsResearchLaboratory,University

ofCalifornia,SantaBarbara,California93106,CenterforLifeDetection,JetPropulsionLaboratory,CaliforniaInstituteofTechnology,Pasadena,California91109,andStanfordSynchrotronRadiationLaboratory,StanfordLinearAcceleratorCenter,Menlo Park,California94025

Received October 3, 2008. Revised manuscript receivedJanuary15, 2009.AcceptedJanuary22, 2009.

Withtheirincreaseduse,engineerednanomaterials(ENMs)will enterthe environmentwheretheymaybealtered bybacteriaandaffectbacterialprocesses.MetallicENMs,suchasCdSequantumdots(QDs),aretoxicduetothereleaseofdissolvedheavymetals,buttheeffectsofcadmiumionsversusintactQDsaremostlyunknown.Here,planktonicPseudomonasaeruginosa PG201bacteriawereculturedwithsimilartotalcadmiumconcentrationsaseitherfullydissolvedcadmiumacetate(Cd(CH3COO)2)orligandcappedCdSeQDs,andcellularmorphology,growthparameters,intracellularreactiveoxygenspecies(ROS),alongwiththemetalandmetalloidfates

weremeasured.QDsdissolvedpartiallyingrowthmedia,butdissolutionwaslessin bioticculturescomparedto sterilecontrols.Dose-dependentgrowtheffectsweresimilarforlow

concentrationsofeithercadmiumsaltsorQDs,buteffectsdifferedaboveaconcentrationthresholdof50mg/L(totalcadmiumbasis)where(1)thegrowthofQD-treatedcellswasmoreimpaired,(2)themembranesofQD-growncellsweredamaged,and(3)QD-growncellscontainedQD-sizedCdSecytoplasmicinclusionsinadditiontoSe 0 anddissolvedcadmium.Formostconcentrations,intracellularROSwerehigherforQD-versuscadmiumsalts-grownbacteria.Taken together,QDswere

moretoxictothisopportunisticpathogenthancadmiumions,andwereaffectedbycellsthroughQDextracellularstabilization,intracellularenrichment,and cell-associateddecay.

Introduction

Therapiddevelopmentoftheengineerednanomaterials(ENMs)industry hasr aisedconcernsaboutENM releases to

theenvironment(1)wherebacteriaareabundant(2)andcancatalyzeessential nutrient-recyclingreactionsduringgrowth(3) andinfluenceENMfates (4). ReportedindividualENM-bacterialbiophysicalinteractionsincludebiosorption,ENMbreakdown(5),andcellularuptake( 6),witheffectsincludingmembranedamageandtoxicity(7,8).However,suchinteractionsarerarelyevaluatedinconcertandovergrowth-associatedtimescales.ThisleavesquestionsaboutENMfatesandeffectswhenbacteriaarepresent,includingthequantitativeimportancetotoxicityendpointsofintact

ENMsversusbreakdownproducts.For heavy metal-composed ENMssuch as cadmium

selenide(CdSe)quantumdots(QDs),toxicmetalionsmaycausecellulartoxicity(9).CdSeQDsarefluorescentsemi-conductorENMsofinterestinphotovoltaics( 10)andindiagnosticsforstablylabelingmammaliancells( 11)andbacteria(12).CdSeQDsareoftencappedwithZnStoenhancefluorescence(13);core-shellconfigurationsalsostabilize

Cd(II)surfaceatomsagainstdissolutionwhichincreasesbiocompatibility(9,14).Still,thereareconcernsaboutcaploss(9,15)andthesubsequenttoxicityofbareQDsanddissolvedcadmium.Cd(II) causescellular toxicity by several mechanisms

includinginterferingwithDNArepair(16)andmetabolicproteins(17),membrane lipidperoxidation (18), substitutionforphysiologicalZn(II),andreactiveoxygenspecies(ROS)formation(19). In gram-negativebacteria, Cd(II) readilyentersthecellthroughopengateMg(II)transporters.Effluxthroughcadmium-inducedmembraneproteinsisthepri-maryresistancemechanism(20).QDsalsogenerateROS,whichdamagemembranes(21);suchdamagemayaccountforQDsnonspecificallyenteringbacteriainthedark( 22)andinthelight(12).Onceincells,QDtoxicitymayagainbefromeitherintactnanoparticles(12)orfromreleasedCd(II)ions(23).However,stillunknownaretherelativetoxicitiesandfatesof Cd(II)ionsversuse itherabsorbedor assimilated

intactQDs,especiallywhentheyco-occurinthebacterialgrowthenvironment.Theobjectivesofthisstudyweretoquantifytheeffects

tobacteriaof ligandcappedCdSeQDsandCd(II)ions, takingintoaccountthatCd(II)ionsmightbegeneratedduringbacterialgrowthifQDsdissolve,andthatQDsmayalsobedirectlytoxic.Weasked:towhatextentdoQDsdissolveinbacterialculture?AreQDsand/orCd(II)ionsassimilatedbycells?Whatis thetoxicityof Cd(II)ions versusQDs?AssumingthatQDs wouldbe toxicdueto dissolvedcadmium,we grewa relativelycadmium-tolerantbacterial strain,PseudomonasaeruginosaPG201,withmeasurablyhightotalcadmiumthatwasinitiallyintheformofeitherCd(II)ionsorQDs.Citratecapped,asopposedtocore -shell(i.e.,metalcapped),QDswereusedto increasethe likelihoodthatboth Cd(II) andQDswouldcoexistin culture,thusprovidingtheopportunitytodifferentiateENMeff ectsfromheavymetaltoxicity.It hasbeenpreviouslyreported( 15,21)thatcappedQDswithno

dissolvedCd(II)causetoxicity,butthe relativeeffectsof both

intactQDsanddissolvedCd(II)havenotbeenevaluateduntilnow.BacteriawerealsogrownwithsolublecadmiumsaltstoseparatelyquantifytheeffectsofCd(II)ions.While

*Correspondingauthore-mail:[email protected];tel:805-893-3195;fax:805-893-7612.

DonaldBrenSchoolofEnvironmentalScience&Management,Universityof California,Santa Barbara.

Departmentof Chemistryand Biochemistry, UniversityofCalifornia,SantaBarbara.

CenterforLifeDetection,JetPropulsionLaboratory,CaliforniaInstituteofTechnology.

| Stanford SynchrotronRadiation Laboratory,Stanford Linear

AcceleratorCenter.

EarthSciences,UniversityofCalifornia,SantaBarbara.# MaterialsResearchLaboratory,UniversityofCalifornia,SantaBarbara.

Environ.Sci.Technol. 2009, 43, 25892594

10.1021/es802806nCCC:$40.75 2009AmericanChemical Society VOL. 43, NO. 7,2009 / ENVIRONMENTALSCIENCE&TECHNOLOGY9 2589

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CdSeQDsdid dissolveinbacterial growthmedia,dissolutionwasincomplete.AfteraccountingforeffectsofCd(II)ions,theresidualtoxicityfromintactQDswasrelativelygreaterthantoxicityfrom cadmiumsaltsalone. Thiswork thusrevealstheseparableeffects of QDsand theirreleasedheavymetals,andnewlyevaluatestheeffectsofENMsonanimportantopportunisticpathogen.

ExperimentalSectionChemicalsandBacterialCulturing. Pseudomonasaerugi-

InstrumentcalibrationwasagainstcommercialCdandSestandards(SigmaChemical).

QDIntegritybyXRDandXANES;andAbioticDissolu-tion. AbioticQD dissolution (seeSupporting Information)wasmeasured.QD intracellularintegritywas inferredin twoways:usingX-raydiffractionforcell-associatedQDcrystalstructure,andusingXANESforcellularSeoxidationstate.Se-K-edgeXANESspectrawerecollectedattheStanfordSynchrotronRadiationLaboratory(SSRL)beamline11-2underSPEAR3todeterminetheoxidationstateofSe,using

overni ht-shi ed(dr ice)tri l icatecell elletsfromaCdSe

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nosa PG201,awell-studiedenvironmentalstrain(24),wasculturedwitheitherCd(II)orCdSeQDsinLuriaBertrani(LB)broth.Allchemicalswerereagentgradeor better(SigmaChemical,St.Louis,MO;andFisherScientific,Hampton,NH). See Supporting Informationfor QD synthesis andculturedetails.

Cultureswere amendedwith either cadmiumacetate(Cd(CH3COO)2 at5,10,20,37.5,75,115,and150mg/Lascadmium)orCdSeQDs(10,20,37.5,50,75,100and125mg/Lascadmium).Controlsincludedmedium-only(nocadmium)anduninoculatedversionsofeachtreatment. Fiveindependentreplicateswerepreparedforeachtreatmentandcontrol.Cultureswerepreparedin200Lvolumesin96-wellmicroplates(seeSupportingInformationfordetails).At6 hafter inoculation,3 replicatesweresubsampledbyasepticallyremoving2 LforCd(II)ionquantification(seebelow).Totesttheeffectsofcitrateongrowth(atconcentra-tionsatandabovethosepresentwiththeQDs),anadditional

treatmentinvolvedamendingLB brothwith400,800,or 1200mg/Lsodiumcitrate.GrowthexperimentswithCd(CH 3COO)2 andCdSeQDs

wererepeatedindependentlyusinglargervolumes(7.5mL)and selected cadmium concentrations (with at least 3replicates)formicroscopy,analysesof intra-and extracellular

metalsandmacromolecules,andanalysisof intracellularROS.Theoptical density (OD) was monitored (600 nm)todetermineif experimentalscale-upcreatedbias. Anothergrowthexperimentwasforassayingacidificationbymea-suringthepH at 0 and 24h for the control and theCd(CH3COO)2 andCdSeQDtreatmentsamendedwith75mg/Ltotalcadmium.Separate7.5mLcultureswerealsogrowntostudyselenium-onlyeffectsusingsodiumselenite(Na2SeO3)overa concentrationrangeupto 500mg/LSe(IV).

CellHarvesting. TodeterminethedistributionofCd(II)ionsversusintactQDsinbacterialculture,lateexponentialphase (24h) cultures of the75 mg/L (total cadmium)Cd(CH3COO)2 andCdSeQDtreatmentswereharvestedforquantifyingtotalcellularmetalandmetalloidcontentsbyinductivelycoupledplasmaatomicemissionspectroscopy(ICP-AES),analyzingSeoxidationstatebyX-rayabsorption

nearedgespectra(XANES),electronmicroscopy,epifluo-rescencemicroscopy,andfordeterminingthecrystalstruc-

tureof intracellularmetalandmetalloidby X-raydiffraction(XRD).Intracellularbiomacromoleculeswerealsoassayed(seeSupportingInformation).

IntracellularROS. TotalROSinabioticCdSeandcad-miumacetatesolutions,andinmidexponentialphase P.aeruginosacultures,werequantifiedusingthe2 ,7-dichlo-rofluoresceindiacetate(DCFH-DA)assay( 25,26)(seeSup-portingInformationforassaydetails).

TotalandDissolvedCadmiumQuantification.DissolvedcadmiumwasquantifiedbytheMeasure-iTkit(Invitrogen,Carlsbad,CA).CalibrationstandardswerepreparedusingCd(CH3COO)2 (0,25,50,75,and100mg/Lascadmium)inallrelevantaqueousconditions:nanopureH2O,sterileLB,andfilter-sterilized(0.2 m)lateexponentialphase(24h)culturesupernatant.ICP-AESwithaTJAHighResolutionIRISinstrument(ThermoElectronCorporation,Waltham,MA)wasusedtoquantifytotalseleniumandcadmium.

QD(75mg/L)treatmentfor24h culturesas describedabove.DetaileddescriptionsoftheXANESandXRDmethods

arelocatedintheSupportingInformation.MicroscopyandImageAnalysis.Phase-contrastmicros-

copy(NikonE800at1000 totalmagnification,withimageacquisition)wasusedformeasuring(inmicrographsusingPhotoshop5.5)the cellaspectratiosoftencellspertreatmentforculturealiquotsdispenseddirectlyontomicroscopeslides.Total cell counts were determined by epifluorescencemicroscopyofcellsfromseparatelygrownlateexponentialphasecultures(LBcontrolsand75mg/LtotalcadmiumaseitherQDs or Cd(II)ions) that were SYBR gold-stained(Invitrogen,Carlsbad,CA)andcountedasbefore(27).High-resolutionmicroscopywasusedto assessmembrane

integrityandmetal,metalloid,andQDlocalizationincells.Scanning transmission electron microscopy (STEM) andenergydispersiveX-rayanalysis(EDXA)wereperformedusing24h culturesforthe75mg/L(total cadmium)QDandCd(II)

treatmentspluscontrols.SeetheSupportingInformationforsamplepreparationandinstrumentdetails.STEMmicrographswereanalyzedinAdobePhotoshop

forcellandnanoparticledimensions,nanoparticlecounts,andmembranedamagefrequency.Celldimensionsweremeasuredfromlongitudinalandverticalcrosssections(5

each),andcellsurfaceareasandvolumeswerecalculatedassumingcylindricalgeometry.

DataAnalysis.CellularSeandCdcontentswerenormal-izedtocellcountsasbefore(27).Statisticalanalyseswereperformedwith SPSS 12.0.1 (SPSS Inc., Chicago, IL) orMicrosoftExcel2 000software.Meanswere comparedby theStudent t test. Where applicable, standard errors werepropagatedaccordingtostandardmethods(28).

ResultsBacterialGrowth and Relationship to QD Dissolution.Growth of P. aeruginosa PG201 was inhibitedby bothCd(CH3COO)2 (FigureS1)andCdSeQDs(FigureS2)inthatincreasedtotalcadmiumresultedinlongerlagtimes,lowerspecificgrowthrates,andlower yields(TablesS1,S2).Growthparametersappearedrelated tototal cadmiumconcentration

similarlyforQD-treatedandCd(CH3COO)2-treatedcultures(TablesS1andS2).ThepHwasconstantduringgrowthandaveraged7.4 ( 0.1.Neithersodiumcitrate(FigureS3),norsodiumselenite(datanotshown)inhibitedgrowth.BecausegrowthwitheitherQDsorCd(CH 3COO)2 ap-

peared similar (Figure S1and S2;TablesS1 andS2),completeQDdissolutionwasimplied.Still,severaltestswereperformedtoquantifyQDdissolution:(1)adialysisstudyof initialdissolutionkineticsinwater(SupportingInformation2.2;FigureS4); (2)dialysis studiestodetermineaqueouschemistryeffectson24hdissolutionendpoints(SupportingInforma-tion2.2;FigureS5); and(3)Cd(II)ionquantificationinculturesat6h,i.e.,entryintoexponentialphaseformostcultures.Mostrelevantto growth,QDswere between 25 and50%dissolvedinculturesat6h(FiguresS1andS2earlyexponentialphase),andtherelationshipbetweenthetotalanddissolvedfractionwasexpectedlylinear(FigureS6).Relatingspecificgrowthratestotheconcentrationof

dissolvedCd(II)at6h(i.e.,endoflagphase)revealedthat

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QD-versusCd(CH 3COO)2-treatedcultureswere similarlyaffectedatlowertotalcadmiumconcentrations(Figure1).However,fordissolvedcadmiumconcentrationsexceedingapproximately20mg/L(i.e.,totalQDcadmium50mg/L)growthratesofQD-treatedculturescontinuedtodeclinesteeplyasafunctionofCd(II)dosewhilegrowthratesforCd(CH3COO)2-treatedcultureswerelesssensitivetocad-miumdose(Figure1).WhenplottedagainstdissolvedCd(II),the other growth curve metrics of lag time and yield(maximumOD)alsoshowedstrongereffectswithQDsincomparisontoCd(CH3COO)2 (FigureS7).

CellularMorphologyandEstimatedIntracellularNano-particles.Above50mg/Ltotalcadmium,QD-andCd(CH 3COO)2-

averageof1.87(0.16105nanoparticlespercell. Intra- andextracellularquantumdotconcentrationswerecalculatedusingthelattercountsaswellasthemeasuredextracellular

concentrationsof totaland dissolvedcadmium(SupportingInformation2.3).Nofurtherevaluationwasmadeofthecadmium-richinclusionswithin Cd(CH3COO)2-treatedcells.

Metal,Metalloid, andBiomacromolecule Contents.Forculturesgrownwith75mg/Lcadmium,totalintracellularcadmium(byICP-AES)at24h(earlystationaryphase)wassimilarforQD-andCd(CH3COO 2)2-treatedculturesandaveraged0.15 ( 0.02pgcell-1,whichwasapproximately4%of thatadministered.Assumingcelldimensions(fromSTEMimages)andcounts(fromepifluorescentmicroscopy),theintracellularconcentrationofthisdissolvedCd(II)wasthenapproximately335g/L,whichwas4460timeshigherthanthe medium.Cellsgrown with QDs(75 mg/L) hadanintracellular Se content (by ICP-AES) of 0.08(0.01pgcell-1,

whichappeared,byXANES,tobemainlySe0

orotherreducedorganoseleniumcompounds(FigureS10).BybothICP-AESandtheMeasureiT assay,all of theintracellularCd(II)appearedto bedissolved(TableS3).However,a relativelyweakXRDpeakat2 24 supportedthatcellscontainedatleastsomeintactCdSecrystals(FigureS11).Thispeakisconsistentwiththe dominantpeakfor CdSeQDssynthesizedaccordingtothesamemethodsthatweused(29).However,thispeakwasonlyslightlyabovebackground,andotheridentifyingpeakswerelikelyobscuredbythedominantAlpeaks.QDand Cd(CH3COO)2-treatedcells hadgreater amounts

of intracellularprotein,DNA,andcarbohydratesascomparedto control cultures (Supporting Information 2.4). Also,comparedto sterilecontrols, QDsin cultureswere lessdissolved(68.5%vs59.7%,respectively)after24h,whichimpliedsome extracellularQD stabilizationin cultures(TableS3).

IntracellularROSandMediaROS.Aftercor rectingforbackgroundfluorescence(fromDCFH,butnotfromeithercellsorQDswhichdidnotinterfere),andconvertingDCFHfluorescencetoH2O2 equivalents,neitherQDsnorcadmiumsalts at 10mg/L total cadmium resulted in measurable

FIGURE 1. Specific growth rate o f P. aeruginosa versusdissolved cadmium amended as either cadmium acetate(squares)orCdSeQDs(diamonds).Asshowninthegraph,allcadmiumtreatmentsresultinreducedgrowthratesrelativetothe no-cadmium control (dark circle). At QD concentrationsexceeding50 mg/L(total cadmiumbasis),QDs remainrelativelytoxicwhileculturesappear toresist Cd(II)ions.

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grown c u ures a ppeare o r espon eren y o edissolvedcadmiumdose(Figure1).Thusoneconcentrationabovethisthresholdwaschosenforanalyzingcellularsize,morphology,andcomparativemetal,metalloid,andbiom-acromoleculecontentsfortheQDandCd(CH 3COO)2 treat-ments.Usinglowerresolution(i.e.,1000)phasecontrastmicroscopy,QD-growncellswereshorterasindicatedbyloweraspectratios (3.3( 0.2)comparedto either cadmium-treated(3.8 ( 0.3)orcontrol(3.9 ( 0.2)cells.Usinghigh-resolutionSTEM,cellsculturedwithCd(CH3COO)2appearedsimilar to no-metal controls except for electron densedepositsinandnearthemembranes(Figure2AvsB)that,byEDXA,werecadmium-rich(datanot shown).Cellsculturedwith QDs alsocontainedCd- andSe-rich electrondenseintracellulardeposits(FigureS8)butwerehighlydisfigured(Figure2C).Atotalof54QD-grownand46Cd(CH3COO)2-treatedcellsinSTEMimageswereevaluatedformembranedamage, asdefinedby holes,blebbing,or detachmentof theplasmamembrane fromthece llwall (Figure S9).Most (81%;

n) 44)oftheQD-treatedandfewer(33%; n) 15)oftheCd(CH3COO)2-treatedcellshadmembranedamage(e.g.,Figure2 ).Blebbing(FigureS9B) wasobservedinQD-treated,butnotforCd(CH3COO)2-treatedcells.Nanosizedparticlesappeared throughouttheQD-treated

cells(Figure2C),whileintheCd(CH 3COO)2-treated cellsparticleswereintheperiplasmicspace(Figure2B).Themeanparticlediametersdiffered(ttest,P) 0.00),with8.02 ( 0.24nmand14.99 ( 0.54nmfortheQDandCd(CH 3COO)2treatments,respectively.BecausethenanosizedparticlesintheQDtreatmentsweresimilarinsizetotheadministeredQDs(5nm),theseparticleswerecounted,resultinginan

n race u ar a er o grow . owever, a ca m umconcentrationsspanning20 through125mg/L,cellularROSwassignificantlygreaterforQD-versusCd(II)-growncells(Figure 3).Abiotic ROSgeneration wasgreaterforQDs inLBthanforQDsinwater(detailedinSupportingInformation2.5).LBalonealsogeneratedROS,butatamuchlowerconcentrationthanforeitherLBorwaterplusQDs(Sup-portingInformation2.5).Aftercorrectingforbackgroundfluorescence(asabove)

andagainconvertingfluorescencetoH2O2equivalents,sterileLBbrothplusDCFHyieldedanROSconcentrationof534 (183mg/LH2O2.WhenaddedtoeitherLBortowater,CdSeQDsalsogeneratedROSabiotically,albeittoamuchlesserextentinwaterascomparedtoLBbroth(FigureS12)andtoamuchgreaterextentthanLB alone(above).CadmiumsaltsaddedtoeithersterileLBorwaterdidnotresultinROSformation.Thepatternof ROSversuscadmiumconcentrationwassimilarwhencomparingthebiotic (Figure3) andabiotic

(Figure S12) QD treatments, with the exception of thedecreaseat125mg/Lcadmiumfortheabiotictreatments.

Discussion

PriorreportsforCdSeQDssuggestthatsurfacecapandsolutionchemistrymodulatetoxicityfrom cadmiumions(9,15).YetZnS-capped,i.e.,coreshell,CdSe( 15)andCdTe(21)QDsthatdidnotreleasecadmiumionswerestilltoxic,andPEG-modifiedCdSeQDswer eto xictomammaliancellsinadose-dependentfashioncorrespondingtointracellu-larizedQDs(23).Intheenvironment,variousabioticandbioticfate-relatedprocessesaffectingENMphasedistribution

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