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7/30/2019 Effects of Soluble Cadmium Salts Versus CdSe Quantum Dots on the Growth of Planktonic Pseudomonas Aerugino
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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:holden@bren.ucsb.edu;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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7/30/2019 Effects of Soluble Cadmium Salts Versus CdSe Quantum Dots on the Growth of Planktonic Pseudomonas Aerugino
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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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8/21/13 Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonic Pseudomonas aeruginosa | Patricia A. Holden - Academia.edu
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8/21/13 Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonic Pseudomonas aeruginosa | Patricia A. Holden - Academia.edu
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8/21/13 Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonic Pseudomonas aeruginosa | Patricia A. Holden - Academia.edu
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