海洋赤潮藻球形棕囊藻在氮磷富营养下的细胞增殖（英文）

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生态环境学报2009,18(2):447-452http://www.jeesci.comEcologyandEnvironmentalSciencesE-mail:editor@jeesci.comCellproliferationofPhaeocystisglobasa,aredtidecausativemarinemicroalgainvariousphosphorus(P)-andnitrogen(N)-repleteconditions*CaiZhuoping,HuangWeiwei,DuanShunshanInstituteofHydrobiology,JinanUniversity,Guangzhou510632,ChinaAbstract:Phaeocystisglobosa,aprevalentbloom-formingmicroalgalspecieswasgrowninvariousphosphorus(P)-repleteandni--3-1-3-1-3-1-3-1trogen(N)-repleteconditions,1P1N(f/2medium):P=5×10g·L,N=75×10g·L;3P1N:P=15×10g·L,N=75×10g·L;1P3N:-3-1-3-1-3-1-3-1P=5×10g·L,N=225×10g·Land3P3N:P=15×10g·L,N=225×10g·L,anditscellgrowthwasmeasuredbyusingchloro-phyllfluorescencedeterminationandcell-countingmethods.TheresultsshowedthatgrowthcurvesofPhaeocystisglobosaexposedeachnutrientconditionsexhibitedas“S-shaped”curvesthroughouttheexperiment,indicatingthemicroalgalcellsexperiencedthreegrowthstages,namelyslow-growthstage,fast-growstageandstationary-growthstage.Chlorophyllfluorescencewasaffectedobvi-ouslybythePand/orNconcentrations.Significantlyhigherchlorophyllfluorescencewasobservedinthe3P1N,1P3Nand3P3N-1-1(above900μg·L)ascomparedwiththanthatin1P1N(only850μg·L),buttherewerenosignificantdifferencesinthechlorophyllfluorescenceamong3P1N,1P3Nand3P3Nconditions.Besides,remarkablyhigherspecificgrowthratewasfoundin3P3Nand-1-1-13P1Nconditions(bothabove0.77d)than1P1Nand1P3Nconditions(only0.70dand0.69drespectively).Finally,changesinthecelldensityofPhaeocystisglobosaexposedtodifferentphosphorus-repleteandnitrogen-repleteconditionsintheterminationofexperimentwereconsistentwiththechangesinchlorophyllfluorescence,withtherelativelyhighercelldensityin3P1N,1P3Nand3P3Nconditionsthan1P1N.OurresultsdemonstratethathighconcentrationofPor/andNinthewaterisamajorfactorresponsibleforthefastgrowthofmicroalgalcells,andthatmeasuringthechlorophyllfluorescenceinmicroalgalcellsisaquick,simple,sensi-tiveandreliablemethod,henceitshouldbeutilizedinthepredictingandmanagingredtides.Keywords:Phaeocystisglobosa;cellproliferation;phosphorus;nitrogenCLCnumber:X171.5Documentcode:AArticleID:1674-5906（2009）02-0447-06RedtideshavedrawngreatattentionbecauseofofstudieshaveprovedthatPhaeocystisisaprodi-theirassociationwithkillingoffishes,poisoningofgiousproducerofDMSP,acrylicacid,andthevolatilemarinewildlife,harmingofhumanhealth,anddegra-DMS,thelatterbeingasalientgreenhousegasinthe[1-3]dationofecosystemalongthecoastalareas.Strongglobalsulfurcycleandaprecursorforatmosphericevidenceisalsopresentedthatthefrequency,intensityparticlesandcloudcondensationnuclei.Besides,anddistributionofredtideshavebeenincreasingPhaeocystiscolonieshavehighC/NandC/Pratios,[4]dramaticallyinrecentyears.Phaeocystisisagenusthereforetheycanremovemoredissolvedinorganicofmarinephytoplanktonwithaworldwidedistribu-carbonperunitofnutrientsassimilatedanddrivethetion,withspeciessharingapolymorphiclifecycle‘‘biologicalpump’’toremoveatmosphericCO2moreincludingfree-livingsinglecellsandcolony-formingefficientlythanotherphytoplankton.Besides,various[5]cells.InChina,adensebloomofPhaeocystisglo-negativeeffectsofbloomofPhaeocystisonhigherbasawasfirstrecordedinthecoastalwatersofsouth-trophiclevelsofcommercialinterests,likefishing,[7-9]eastChinain1997;afterthenfrequentPhaeocystisaquafarmingandtourismhavebeenreported.Onglobasa-formingredtidescontinuedtoberecordedintheotherhand,althoughagreatdealofworkhasbeen[6]1999,2000,2003,2004and2005.Agreatnumberdoneintermsofredtides,theiroutbreakmechanisms基金项目：国家自然科学基金项目（40876074,30770336）；广东省科技计划重点引导项目(2005B33201001)；珠海市科技计划重大项目(PC20061045)作者简介：蔡卓平(1980年生)，男，博士研究生，研究方向为海洋环境与赤潮及微藻生态与生物技术。E-mail:zpcai@scau.edu.cn*通讯作者收稿日期：2008-12-14 448生态环境学报第18卷第2期（2009年3月）areverycomplexandhavenotbeenfullyunderstoodlightcycle.Theexponentially-growingcellswerein-uptonow.Theoutbreakofredtidesisbelievedtobeoculatedintoidentical50mLtesttubes(SchottDuran,associatedwithsomecomplexecologicalandocean-Germany)containing35mLsolutionandmaintainedographicalprocesses,anditisalsoaffectedbyavari-intheshakerunderthegrowthconditionsasdescribed[10]etyofenvironmentalfactors.Amongthem,waterbefore.Fournutrientconditionswereachievedbytemperature,salinityandlightarethoughttobetheaddingdifferentamountofNaH2PO4or/andNaNO3mostbasicfactorsforthesurvivalandreproductionofintothegrowthmedium,whichweredenotedas1P1N[11-13]redtideorganisms.Phosphorus(P)andnitro-(f/2medium,asthecontrol),3P1N,1P3Nand3P3Ngen(N)aretwoessentialmacronutrientsrequiredinaslistedinTab.1.Chlorophyllfluorescencewasmeas-plantgrowthanddevelopment.SomerecentstudiesuredeverydaybyusingTD-700fluorometer(TurneralsohaveshownthatexcessivePor/andNenrich-Designs)duringtheexperimentalperiod.Maximummentsviaindustrialandagriculturalinputsintothespecificgrowthrateofsamplesdeterminedtobeinaquaticenvironmentsplayaparticularlyimportanttheexponentialgrowthstagewascalculatedbyleastroleinthecellproliferationofmicroalgae,resultinginsquaresfitofastraightlinetothedataaftertheyhadmassiveoccurrenceofredtidesalongthecoastalwa-beenlogarithmicallytransformedbasedonthefol-[14-15]ter.Inthepresentstudy,weevaluatethecelllowingequation:µ=(lnX2-lnX1)/(t2-t1),whereX1andgrowthofP.globosagrowninvariousPor/andNX2arethechlorophyllfluorescencevaluesatdayt1concentrationsbymeasuringchlorophyllfluorescenceanddayt2.Intheendofexperiment,a0.5-mlalgalofmicroalgalcoloniesandcountingthemicroalgalsolutionwassampledandthenumbersofalgalcellcellnumber.Thesefindingswillbeimportantforun-werecountedunderaopticalmicroscope(OLYMPUSderstandingthemechanismsbehindmassiveoccur-CX41)afterpreservedwithLugol’ssolution.Eachrenceofredtide,andfordevelopingsomeusefulcellsamplecountingwasrepeatedatleastthreetimesmethodsforpredictingandmanagingthefrequentredandaveraged.Allexperimentswerecarriedoutintideevents.triplicateforeachtreatment,andthetubescontaining1MaterialsandMethodsmicroalgalcultureswereshakengentlytwiceeveryPhaeocystisglobosa,afrequentbloom-formingday.microalgalspecies,wasobtainedfromtheInstituteofTable1NutrienttreatmentsdifferentinphosphorusandHydrobiology,JinanUniversity,Guangzhou,Chinanitrogenconcentrationsusedintheexperimentandroutinelymaintainedinaplantgrowthcham-Nutrientconcentration1P1N(f/2,control)3P1N1P3N3P3N-1-3-3-3-3ber(CC275TL2H,Hangzhou,China)understandard-Phosphorus(g·L)5×1015×105×1015×10-1-3-3-3-3Nitrogen(g·L)75×1075×10225×10225×10izedconditionattheconstantirradiance(5000lx)andtemperature(22±1)℃ina12h/12h(light/dark)pho-2Resultstoperiodcycle.Artificialseawaterwaspreviouslyfil-ThechangesingrowthcurvesofPhaeocystisteredthrough0.45µmporosityfiltersandaddedwithf/2enrichmentsolutionformicroalgalcultures[16].globosaculturedinvariousnutrientcircumstanceswereillustratedinFig.1.Inthebeginningoftheex-Algalcellsinexponentialgrowthphasewereem-periment,Phaeocystisglobosagrewquiteslowly,ployedfortheexperiments.AllglasswareandmediawhiledramaticalfastgrowthofPhaeocystisglobosaconnectedwiththeexperimentswerepreviouslyster-ndthcellscouldbeobservedfromthe2daytothe5day,ilized.Salinityoftheartificialseawaterwas30‰andafterwhenthechlorophyllfluorescenceofPhaeocys-theinitialpHoftheculturewas6.5~7.0.Priortothetisglobosashowedarelativelystableincreasetotheexperiments,inordertominimizeotherenvironmentalteminationoftheexperiment,withthegrowthcurveseffectsonthegrowthofmicroalgalcells,pre-cultureexhibiting“S-shaped”curvesthroughtouttheex-wascarriedoutinashaker(IncubatorShakerSeries,periment.However,itwasevidentthatchlorophyllInnova44,NEWBRUNSWICKSCIENTIFIC)with80rpmat23℃and80µmol·m-2·s-1downwardir-fluorescenceofPhaeocystisglobosagrowninthe1P1Nremainedatthelowestlevelduringtheexperi-radianceprovidedbycool-whitefluorescentlampsment,ascomparedwithotherthreenutrientconditions.fixedonthetopeofshakerwitha12h:12hdark: 蔡卓平等：海洋赤潮藻球形棕囊藻在氮磷富营养下的细胞增殖44910001P1Nglobosawasfoundinthenutrientconditionsof3P1N-19003P1Nand3P3N,bothamountingtoapproximately0.77d,1P3NbutthespecificgrowthrateofPhaeocystisglobosa800)3P3Ngrowninthe1P1Nand1P3Nconditionsonlycameto700g•L-1μ-1-1about0.70dand0.69drespectively.600ThedifferencesinthecelldensityofPhaeocystis500globosaculturedinvariousnutrientconditionswere400presentedinFig.3.Phosphorusandnitrogennutrient300Chlorophyllfluorescence/(hadsignificanteffectsonthecelldensity.Whenthe200marinemicroalgaPhaeocystisglobosawasgrownin100thef/2medium(1P1N),thecelldensityintheendof04-1experimentonlyaccountedfor180×10cell·mL;12345678910Culturetime/dhowever,thecelldensitiesforthePhaeocystisglobosainthe3P1N,1P3Nand3P3Nconditionswerein-Fig.1GrowthcurvesofPhaeocystisglobosaunderdifferent4-14-1nutrientconditionsovertime.Eachpointindicatescreasedto220×10cell·mL,216×10cell·mLandthemeanofthreereplicateswithstandarderror237×104cell·mL-1,respectively,significantlythanthecelldenistyofPhaeocystisglobosain1P1N.ButthereForexample,inthelastdayoftheexperiment,thewerenostatisticaldifferencesamongthecelldensitieschlorophyllfluorescencein1P1Nwasonlyabout850ofPhaeocystisglobosagrownunderthe3P1N,1P3N-1μg·L,butthatin3P1N,1P3Nand3P3Nreachedtoand3P3Nconditions.-1above900μg·L,whichwassignificantlyhigherthan300thatin1P1N.Ontheotherhand,Phaeocystisglobosagrownin3P3Nand3P1Nshowedthehighestchloro-)phyllfluorescence,follwedbythatin1P3Ncondition-1200acrosstheexperimentperiod.Butintheterminationofexperiment,therewerenosignificantdifferencesamongthechlorophyllfluorescencevaluesofPhaeo-100cystisglobosaexposedto3P1N,1P3Nand3P3NCelldensity/(×104cell•mLconditions.AsshowninFig.2,specificgrowthrateof0Phaeocystisglobosaexposedtodifferentnutrient1P1N3P1N1P3N3P3Nconditionsvariedsignificantly.ItwasobviousthatTreatmentrelativelyhigherspecificgrowthrateofPhaeocystisFig.3CelldensityofPhaeocystisglobosaunderdifferentnutrientconditionsintheterminationofexperiment.Eachpointindicates0.9themeanofthreereplicateswithstandarderror3Discussions0.6SomespeciesofmarinemicroalgaeproliferateorassemblesoquicklyundersomegivenconditionsthatSGR/dtheycangivebrownishyelloworreddishcolortothe0.3entirebodyofwaterdependingonthealgaeinvolved,[17]whichisbestknownasredtides.Ithasbeenwelldocumentedthatredtideshaveincreasedinthefre-01P1N3P1N1P3N3P3Nquency,intensityandgeographicdistributionduringTreatmentthelastdecades[18].Let’stakeChinaforexample.InFig.2SpecificgrowthrateofPhaeocystisglobosaunderdifferent2001,77-timeredtideeventswererecordedandthenutrientconditionsduringtheexponentialgrowthstage.Eachpollutedareawasover15000km2,whichwasanin-pointindicatesthemeanofthreereplicateswithstandarderror2creaseof49timesand5000kmascomparedwith 450生态环境学报第18卷第2期（2009年3月）thosein2000.ThegeographicdistributionofredtidecialroleinthefastgrowthanddivisionofmicroalgaloutbreakcoveredtheEastSea,BohaiSeaandYellowcells.Inthepresentstudy,thef/2medium,alsode-[19]SeaofChina.Ontheotherhand,frequentoccur-scribedas1P1N,wasusedasthecontrol.Infact,lowrencesofredtideshavebeenreportedtodestroythenutrientlevelsofPorNhavebeenprovedtorestrictnaturalmarineecosystems,affectthethegrowthofmicroalgalcellssignificantlyascom-socio-economicalactivitiesandinflictsignificantlyparedwiththef/2medium,whichisbelievedtomeet[20]negativeimpactsonthehumanhealthy.Asitisthebasicnutrientdemandformostofmicroalgalknownthatlowlightpenetration,highrespirationorgrowth.Ourresultsalsoindicatedthat1P1Ncansat-massivedecayofredtideorganismsasaconsequenceisfythegrowthandproliferationofPhaeocystisglo-ofoverproliferationoroverassemblagewillleadtobosaduringthewholeexperimentalperiod,andthreegreatoxygendepletioninthewaterbody,thuscausingobviousgrowthstages,namelyslow-growthstage,deleteriousdecreaseoffishcatchorincreasedmortal-exponential-growthstageandsteady-growthstageityofbenthicorganisms.Inaddition,unpleasantap-werefinished.Butinotherthreenutrientconditions,pearanceandtasteofthewaterbodywillresultfrom1P3N,3P1Nand3P3N,containingmuchmorePthedevastatingredtides,leadingtothelossesofrec-or/andN,Phaeocystisglobosastillshowedanin-reationalresources.Whatisworse,someredcreasingtendencyincellgrowth,suggestingthattide-causativemicroalgaehavethepotentialtopro-higherPor/andNconcentrationscouldstillpromotducetoxins,andthetoxicandlethalsubstancespro-thecellgrowthtoacertaindegree.Forexample,intheducedbysuchmicroalgaecanbringaboutmassdeathendofexperiment,thechlorophyllfluorescenceofofaquaticanimals,likesomefishes,shrimps,crabsPhaeocystisglobosagrowninthe1P1N(f/2medium)-1andsoon;insomecases,itcanalsobringaboutthewasonlyabout850μg·L,butthechlorophyllfluo-poisoningofhumanbeings.Forinstance,aredtiderescenceofPhaeocystisglobosagrowninthehigheroccurredfromthemid-Marchtomid-April,1998innutrientconditions,3P1N,1P3Nand3P3Npeakedat-1thenortherncoastalwatersoftheSouthChinaSea,above900μg·L,andthesimilarincreasingtrendto-includingHongKong.By17April,about1monthwardsincreasingnutrientconditionswasalsocon-aftertheblooming,nearlyallthecornersofthecoastalfirmedbythecelldensitycountings,whichweresig-watersofHongKonghadbeeninvadedandaffected,nificantlylowerinthe1P1N(f/2medium)inthecom-causingabout2500tonnesoffisheskilled,withadi-parisionwithotherthresshighernutrientconditions.recteconomiclossofHK$250million;whileintheHowever,itneedstopointoutthattheratioofPandNMainlandwaters,thisHABshadkilledmorethan260hasalsobeenreportedtobeakeyfactorincontrollingtonnesfishby17April,resultinginadirecteconomicthemicroalgalgrowth,andnextstepsomeexperi-[21]lossofabout40millionYuanRMB.SomefieldmentswillbecontinuedwithmuchmorePor/andNandlaborotorystudieshavebeenconductedontheredconcentrations/ratiosinordertogodeeperintothetidesinthesedecades,andsomeprogresshasbeenroleofPor/andNinthecellgrowthandproliferationachieved,indicatingthattheoccurrenceofredtidesisofmicroalgae.closelyrelatedtothecombinationofphysical,chemi-Thereisnodoubtthatfindingsomenewtech-calandbiologicalfactors,butresearchesontheniquestoquicklypredictthecellgrowthorprolifera-mechanismsunderlyingthemassiveoutbreakofredtionisnecessaryforthebettercontrollingandmanag-tidearestillinanearlystageandagreatamountofingredtides,thusreducingtheharmfuleffectsresult-relevantworkisstillneededtobecontinuedanden-ingfromredtideeventsontheenvironmentandsoci-hanced.ety.Actually,themosttraditionalmethodsaretocountPhosphorusandnitrogenaretwoessentialnutri-thecellnumberofmicroalgalcellsinacertainvolumeentsrequiredbyplantgrowthanddevelopment.Thewaterwiththehelpofmicrocopyandhemocytometer,unceasinginputofthesetwonutrientsintotheriverortomeasuretheopticaldensityofmicroalgalcultureandotheraquaticenvironmentshasbecomethefirstbyusingspectrophotometer.Thesetraditionalmeth-[22]primaryfactorresponsiblefortheeutrophicationofodsaregenerallytime-consumingandtroublesome.waters,andtheyareshowntobeplayingaverycru-Inourstudy,chlorophyllfluorescenceofmicroalgal 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452生态环境学报第18卷第2期（2009年3月）海洋赤潮藻球形棕囊藻在氮磷富营养下的细胞增殖*蔡卓平，黄伟伟，段舜山暨南大学水生生物研究所，广东广州510632摘要：利用常见海洋赤潮微藻球形棕囊藻（Phaeocystisglobosa）为试验研究材料，以f/2海洋微藻营养液为对照（1P1N：磷-3-1-3-1-3-1质量浓度为5×10g·L，氮质量浓度为75×10g·L），设置3组富磷和富氮营养处理（3P1N：磷质量浓度为15×10g·L，氮-3-1-3-1-3-1-3-1质量浓度为75×10g·L；1P3N：磷质量浓度为5×10g·L，氮质量浓度为225×10g·L；3P3N：磷质量浓度为15×10g·L，-3-1氮质量浓度为225×10g·L），利用细胞记数和叶绿素荧光测定等方法研究了藻细胞在不同富磷和富氮条件的增殖情况。结果显示，不同浓度磷和氮营养下的藻体荧光值变化在试验周期内均呈现“S”型曲线，表明藻细胞的生长经历缓慢期，快速期和平缓期3个阶段；同时，不同的富磷和富氮营养条件对球形棕囊藻的叶绿素荧光值有一定的影响，其中在对照1P1N下的藻-1-1体荧光值最低，在试验结束时（第10天）只有850μg·L，而在3P1N,1P3N和3P3N条件下的藻体荧光值均达到900μg·L以上，显著高于1P1N下的藻体荧光值，表明富磷和富氮营养可以促进藻细胞的生长增殖，但在试验设置的不同富磷和富氮营养下的藻体荧光值之间没有显著的差异。就不同磷和氮营养条件下的藻最大比生长速率而言，3P3N和3P1N条件下的最大，均达-1-1-1到0.77d，明显高于1P1N和1P3N条件下的藻最大比生长速率（分别只有0.70d和0.69d）。此外，试验结束时细胞密度的变化趋势与藻体荧光值相似，富磷和富氮营养条件下的细胞密度显著高于1P1N下的细胞密度，而富磷和富氮营养条件下的细胞密度间也不存在显著的差异。研究结果揭示，水体中的高磷和高氮营养浓度是导致藻细胞大量快速增殖的一个主要因素，而利用叶绿素荧光来测定藻细胞增殖是一种快速、简便，灵敏和可靠的方法，可在今后赤潮监测过程中多加利用，以能及时、准确地预测预报赤潮爆发，从而减少其对环境和经济的影响。关键词：球形棕囊藻（Phaeocystisglobosa）；细胞增殖；磷；氮