BaohuaZhua,FaqiangSuna,MiaoYanga,LinLua,GuanpinYangb,KehouPana,⇑abKeyLaboratoryofMariculture,MinistryofEducation,OceanUniversityofChina,Qingdao266003,ChinaCollegeofMarineLifeSciences,OceanUniversityofChina,Qingdao266003,Chinahighlights
ThreeNannochloropsisstrainswerecultivatedsuccessfullyusingfluegas.Lowertemperaturesandilluminationledtolowerbiomassandlipidproductivities.Fattyacidcompositionsofalgalstrain4-38aresuitableforbiodieselproduction.Algalstrain4-38isagoodpotentialsourceforbiodieselproduction.articleinfoabstract
Thepotentialuseofmicroalgalbiomassasabiofuelsourcehasraisedbroadinterest.Highlyeffectiveandeconomicallyfeasiblebiomassgeneratingtechniquesareessentialtorealizesuchpotential.Fluegasfromcoal-firedpowerplantsmayserveasaninexpensivecarbonsourceformicroalgalculture,anditmayalsofacilitateimprovementoftheenvironmentoncethegasisfixedinbiomass.Inthisstudy,threestrainsofthegenusNannochloropsis(4-38,KA2and75B1)survivedthistypeofcultureandbloomedusingfluegasfromcoal-firedpowerplantsin8000-Lopenracewayponds.Lowertemperaturesandsolarirradiationreducedthebiomassyieldandlipidproductivitiesofthesestrains.Strain4-38performedbetterthantheothertwoasitcontainedhigheramountsoftriacylglycerolsandfattyacids,whichareusedforbiodieselproduction.Furtheroptimizationoftheapplicationoffluegastomicroalgalcultureshouldbeundertaken.Ó2014ElsevierLtd.Allrightsreserved.Articlehistory:Received8July2014Receivedinrevisedform22September2014Availableonline30September2014Keywords:BiodieselproductionFluegasNannochloropsisOpenracewaypond1.IntroductionItisclearthattheuseoffossilfuelsisnotsustainableorrenew-ableastheyhavecausedunwantedanddifficulttoremediateenvironmentalchangesandtheirsupplieswillsoonbeexhausted.Asoneofthealternatives,sustainable,renewableandenvironmen-tallyfriendlybiofuelshavebeenhighlyanticipatedandwidelyexplored(Rawatetal.,2013).Microalgaeareapromisingalternateenergysourceastheyarecharacterizedbyhigherlipidproductiv-itiespergroundareathanoleaginousagriculturalcropsanddonotcompeteforarablelandorbiodiversenaturallandscapes(Jietal.,2013).Microalgaeproduce15–300-foldmoreoilforbiodieselproductionthantraditionalcropsonanareabasis(Chisti,2007).⇑Correspondingauthorat:YushanRoad5,Qingdao266003,China.Tel./fax:+8653282031939.E-mailaddress:khpan@ouc.edu.cn(K.Pan).http://dx.doi.org/10.1016/j.biortech.2014.09.1160960-8524/Ó2014ElsevierLtd.Allrightsreserved.Inaddition,microalgalbiodieseloffersauniqueopportunitytocompletelydisplacefuelsderivedfrompetroleum(Chisti,2008).Renewableenergyfrommicroalgalbiodieselhasbeenstudiedfordecades(WijffelsandBarbosa,2010).Unfortunately,agreatdealofdevelopmentmustoccurbeforesuchproductsreachthemarketplace.Oneofthekeybottlenecksisthehighcostofmicro-algalcultivation(Lietal.,2011;Singetal.,2013).Forthesuccessfulcommercializationofmicroalgae-basedfuelsitiscrucialtomini-mizeculturecostandbreedoil-richmicroalgae.(SinghandGu,2010).Variousstrategieshavebeenusedtoreducethecostofpro-ductionofmicroalgalbiomass,suchassequesteringcarbondioxidefromindustrialplantsasthecarbonsource(Douchaetal.,2005;Douskovaetal.,2009),usingwastewaterforthenutrientsupply(Jietal.,2013)andmaximizingthevaluesofby-products(BrennanandOwende,2010).Inadditiontoadequatesuppliesofnutrientsandsolarirradia-tion,theproductionoflargequantitiesofbiomassalsorequiresalargeamountofCO2.Asdocumentedearlier,atotalof1.8tonsof54B.Zhuetal./BioresourceTechnology174(2014)53–59CO2isneededtoproduce1tonofalgalbiomass(Chisti,2007).Thecarbonsourcenecessaryforthecultivationofmicroalgaerepresentsupto60%ofthecostsalongwithnutrients.Thus,itisworthwhileinvestigatingtheuseoffluegasfromcoal-firedpowerplantstoculturemicroalgaetoreducecosts(Zeileretal.,1995;Douchaetal.,2005;Lietal.,2011).Douchaetal.(2005)foundthattheproductioncostsforalgalbiomassmaydecreaseabout15%(representingthepriceofCO2)withpartialdecarbonizationoffluegas.Fluegasesgeneratedfrompowerplantscontain10–15%(v/v)CO2(Zeileretal.,1995)aswellassulfurandnitrogenoxides.ThesecompoundsmaybetoxicforculturegrowthbecausetheyreducethesolutionpHandalsothroughdirectinhibition(Piresetal.,2012).Inotherwords,notallalgalstrainscanbegrownusingfluegasasacarbonsource.Negoroetal.(1991)evaluatedtheeffectsofSOxandNOxonthegrowthoftenstrainsofmarineandhalotoler-antmicroalgae.WithaCO2concentrationof15%,thegrowthofNannochlorissp.andNannochloropsissp.wasnotaffectedby50ppmofSO2.ArelativelyhighgrowthrateofNannochloropsissp.hasbeendocumentedwhen10–15%fluegasorsynthesizedCO2isused(Jiangetal.,2011).Itisimperativethatthestrainselectedforlarge-scalecultiva-tionproducestheappropriatelipidsunderthestressculturecondi-tionssuchasthosethatexistwhenusingfluegasonalargescale.Selectioncriteriashouldbebasedonanumberoffactorsincludinggrowthrate,lipidquantityandquality,strongadaptabilitytochangesinenvironmentanddeterminationofpreferrednutrientsandnutrientuptakerates(Amaroetal.,2011).Culturestabilityisessentialforlarge-scalemicroalgalcultivationandthereforeitisimportantthatcareistakenwhenselectingthespeciesandstrainstoensurethattheyarebestsuitedtotheculturesystemandtheprevailingenvironmentalconditions(Singetal.,2013).Openracewaypondsarehighlyvaluedastheyarenotexpen-sivetoconstructandrunandareconvenienttooperate,andappeartobetheonlysustainableculturesystem(Piresetal.,2012).Thecostofconventionalmediaformicroalgaeproductionmeansthismethodisnotfeasibleforlowvalueproductssuchasoiland,thus,othernutrientsourcesmustbeconsidered(Rawatetal.,2013).Thechoiceofmediaisfundamentaltothesuccessofmicroalgalcultivationatthepilotscalephase.Here,thefocuswasmainlyontheselectionofalgalstrainssuit-ableforcultivationwithfluegasfromcoal-firedpowerplantstoproducebiodieselonalargescaleinopenracewayponds.Anotheraimwastouseanindustrialmediumtocultivatemicroalgaeonalargescaletoreducethecosts.Thusfar,fewstudieshavebeencon-ductedtotestthesuitabilityofgrowingmicroalgaeusingfluegasfromcoal-firedpowerplantsforbiodieselproductiononalargescale,thuscurrentresearcheffortsinthisareaarenecessaryandimportant.2.Methods2.1.NannochloropsisstrainsNannochloropsisoceanicaKA2wasscreenedwithquizalofop-p-ethyl.FiveN.oceanicastrains(3-25,3-26,4-5,4-38and75B1)Fig.1.Schematicdiagramofanexperimentalopenracewaypondforcultivationofmicroalgaeusingfluegas.(a)Coal-firedboiler;(b)electronicaircleaner;(c)forceddraftfan;(d)desulfurizingtower;(e)stack;(f)hydraulicashhandling;(g)airinletinterface;(h)openracewayponds;(i)enlargeddiagramofracewaypond;(j)gasinlet;(k)seawaterinlet;(l)freshwaterinlet;(m)paddlewheelandmotor;(n)seawaterdisinfectingtank;(o)seawatersandfilter;(p)highpoweredwaterpump;(q)freshwatersupplyline.B.Zhuetal./BioresourceTechnology174(2014)53–5955Fig.2.Celldensity(a),OD(750nm)(b)anddryweightbiomass(c)changesduringcultivationofthethreestrains(4-38,KA2and75B1)suitableforfluegasculture.weremutagenizedwithEMSintheLaboratoryofAppliedMicroal-gaeBiology,OceanUniversityofChina,andprovedtobesuitableasrawmaterialsforcommercialproductionduetotheirhighbiomassandoilcontent.2.2.Masscultureofmicroalgaeusingfluegasfromcoal-firedpowerplantsMassculturesofmicroalgaewereundertakeninPenglaiCity,ShandongProvince,China(northlatitude:37.48°,eastlongitude:120.45°),from26Novemberto11December2013.Theywerecar-riedoutintriplicateinindoorracewayponds,eachhavingacapac-ityof2000-L,4000-Lor8000-L,usingfluegasfromcoal-firedpowerplantsthathadbeensubjectedtodust-removinganddesul-furizationtreatment(showninFig.1).FluegascontainingCO2(13%v/v),O2(6.7%),CO(26ppm),NO(115ppm),NOx(129ppm),NO2(14ppm)andSO2(30ppm)wasinjectedintotheculturethroughanundergroundpipelinefrom8:00a.m.to6:00p.m.everyday,atarateof0.17m3minÀ1.Thepaddlewheelspeedwassetat11rminÀ1from8:00a.m.to6:00p.m.everydayduring16daysofexperiments.Thematerials,typesandsizesofthepaddlewheelswerethesameinopenpondsofthesamesize.Inordertoreducethecostofcultivation,themicroalgaewerecultivatedinseawater(25gLÀ1salinity)asanindustrialgrowthmediumcontaining0.2mmolLÀ1(NH4)2SO4and0.17mmolLÀ1KH2PO3.Illuminationwasprovidedbydailysunlight.Microalgalcellsin8000-Lracewaypondswereculturedfor16days.ThecelldensitywasmeasuredeverydayusingMoticImagesAdvanced3.2Software.Theopticaldensity(OD)wasmeasuredeverydaywithaspectrophotometer(HITACHI,U-3310,Japan)at750nm.Thedryweightofeachbio-masswasalsomeasuredeveryday.Attheendofcultivation,algalcellswereharvestedbycentrifugation(PX505,Nanjing,China;5500g,10min)andspraydryingbeforetotallipidandfattyacidcompositionanalysis.Thespecificgrowthratewascalculatedaccordingtotheequa-tionu¼ðlnNtÀlnN0Þ=ðt1Àt0ÞwhereNtandN0aretheOD(750nm)attimet1andt0,respectively.Duringcultivation,thetemperature,pHandlightintensityweremeasuredeverydaythreetimesinthemorning,atnoonandintheafternoonatafixedtime.Itshouldbenotedthatthreealgalstrains(3-25,3-26,4-5)diedoffastheywereunsuitableforfluegascul-tivation.Thus,theotherthreealgalstrains(4-38,KA2,75B1)werecultivatedusingfluegasandtheirgrowthparametersincludingtotallipidsandfattyacidcompositionweremeasured.2.3.LipidproductivityAsperLiuetal.(2011),lipidproductivity(P)expressedasmil-ligramsperliterperdayisgivenby1000CB/D,whereCislipidcontent(%ofDW),Bisbiomass(gLÀ1)andDiscultivationtime(d).2.4.TotallipidsandfattyacidcompositionanalysisTotallipidswereextractedfromspray-driedalgalbiomassusingthemodifiedmethoddescribedbyBlighandDyer(1959).Totallipidswerefurtherseparatedbythinlayerchromatography(TLC)onsilicagelplatesGF254(HAIYANG,Qingdao,China)aspre-viouslydescribed(ReiserandSomerville,1997;Chenetal.,2012).GlyceroltrioleatewaspurchasedfromSigma–AldrichCorporation(St.Louis,MO,USA)andusedasastandard.Lipidswerevisualizedbyexposingtheplatestoiodinevapor(Chenetal.,2012).FattyacidswereanalyzedusingamethodmodifiedbyLepageandRoy(1984).Fattyacidmethylesters(FAMEs)wereanalyzedbygaschromatography(Agilent7820A)withaflameionizationdetector(FID)andAgilentJandWGCcolumns(AgilentTechnolo-gies,USA).Highpuritynitrogenwasusedasacarriergas.Theinjectionvolumeandsplitratiowere1lLand45:1,respectively.Thetemperaturesoftheinjectoranddetectorweresetat250°Cand280°C,respectively,andthecolumnwasprogrammedas56B.Zhuetal./BioresourceTechnology174(2014)53–59Table1Specificgrowthrate,celldensity,biomass,lipidcontentandlipidproductivityofthethreestrains(4-38,KA2and75B1)suitableforfluegasculture.Algalstrains4-38KA275B1Specificgrowthrate(dÀ1)0.047±0.001a0.066±0.005a0.051±0.003aCelldensity(OD750)1.050±0.015a1.139±0.015b1.135±0.057bBiomass(g/L)0.323±0.015a0.316±0.006a0.338±0.015aLipidcontent(%)28.000±1.00c21.400±1.53a25.670±1.33bLipidproductivity(mgLÀ1dÀ1)4.69±0.19c3.23±0.18a4.40±0.16bValuesinthesamelinewithdifferentsuperscriptsaresignificantlydifferent(P<0.05).Valuesaremeans±SD.Fig.3.Averagewatertemperature(a),pH(b)andlightintensity(c)changesduringcultivationofthethreestrains(4-38,KA2and75B1)suitableforfluegasculture.follows:initialtemperature50°C,isothermalfor1min,then25°CminÀ1upto175°C,isothermalfor0min,then4°CminÀ1upto250°Candisothermalfor5min.MixCRM(Supelco37,USA)wereusedasstandards.Eachexperimentwascarriedoutintriplicateandaverageval-ueswerereported.2.5.StatisticalanalysisThesignificantdifferencesbetweentreatmentswerecalculatedwithSPSS20softwareusingone-wayanalysisofvariance(ANOVA)atalevelofsignificanceofP<0.05,andalldataarereportedasmeans±SD.3.Resultsanddiscussion3.1.GrowthandbiomassSixNannochloropsisstrains(3-25,3-26,4-5,4-38,KA2,75B1)wereselectedforcultureusingfluegasfromcoal-firedpowerplantsatthebeginningoftheexperiment.Unfortunately,threealgalstrains(3-25,3-26,4-5)didnotsurviveastheywereunsuit-ableforfluegasculture.Fluegasescontainsulfurandnitrogenoxi-des,andthesecompoundsmaybetoxicformicroalgalgrowthbecausetheyreducethesolutionpHandalsobydirectinhibition(Negoroetal.,1991),whichsuggeststhatnotallalgalstrainscanbegrownwithfluegasasthecarbonsource.Inthisstudy,itwasfortunatethatthreealgalstrains(4-38,KA2,75B1)couldbeculti-vatedsuccessfullyusingfluegasandtheirgrowthparametersincludingcelldensity,OD(750nm)andbiomassweremeasured(Fig.2).Thegrowthparametersofthethreealgalstrainsincreasedwithculturetimeandtheexponentialphaselasteduntiltheendoftheexperiments(Fig.2).Nosignificantdifferenceswerefoundbetweenthespecificgrowthratesandbiomassesofthethreealgalstrains(Table1).Ingeneral,thegrowthratesanddryweightbio-massesfoundinthepresentstudyweremuchlowerthanthosefromotherpublishedstudies(Convertietal.,2009;Moazamietal.,2012).Thisisnotduetouseoffluegasbutrathertolowertemperaturesandlowerlightintensities,astheaveragepHwaskeptconstantduringthe16daysofexperiments(Fig.3b).ThisisinconsistentwiththeresultsdescribedbyPiresetal.(2012),whoreportedthatthesupplyofgasessuchCO2,NOxandSO2reducedthepHoftheculturemedium.AsshowninFig.3,theaveragewatertemperature(a)andlightintensity(c)werealsomeasuredduringperiodsofcultivationofthethreestrains(4-38,KA2and75B1)suitableforfluegasculture.Theaveragetemperaturesfluctuatedbetween5.12±0.24°Cand10.01±0.42°C(Fig.3a).Theaveragehighestandlowestlightintensitieswere355.35±6.54and113.94±2.78lmolmÀ2sÀ1,respectively(Fig.3c).Thelowertemperaturesandilluminationsresultedinslowergrowthratesandlowerdryweightsofbio-masses.Similarresultshaveindicatedthatthelimitofbiomassyieldperunitlanduseddependsonlightavailabilityratherthanontheintrinsicgrowthrate(Sforzaetal.,2012).B.Zhuetal./BioresourceTechnology174(2014)53–5957Fig.4.Analysisofthetotallipidsextractedfromthethreestrains(4-38,KA2and75B1)suitableforfluegasculturebythinlayerchromatography.Insomecases,cellshavetobeculturedwithalight–darkcycle.Forexample,fortheproductionofbiofuelsfrommicroalgae,out-doorculture(orindoorculturewithnaturalsunlight)iswidelyappliedtoachievelow-costandlarge-scalecultureofoil-produc-ingmicroalgae.However,biomasslossduringthedarkperiodwaspartlyresponsibleforaslowgrowthrateandlowbiomass(Hanetal.,2013).3.2.TotallipidsandlipidproductivitiesTriacylglycerols(TAGs),themajorfeedstockforbiodieselpro-duction,areneutrallipidsmainlystoredinvacuoleswithinthecell.AsindicatedinFig.4,algalstrain4-38producedmoreTAGsthantheothertwostrains(KA2and75B1).AsfaraslipidproductivityandTAGsareconcerned,cultureofalgalstrain4-38withfluegasfromcoal-firedplantsisagoodpotentialsourcefortheproductionofbiodieselunderthecondi-tionofthisstudy.3.3.FattyacidcompositionsuitableforbiodieselproductionAsindicatedinTable1,totallipidsproducedbyalgalstrain4-38weresignificantlyhigherthanthoseofalgalstrainsKA2and75B1.However,totallipidsofthethreealgalstrainsweresignificantlylowerthanthoseobtainedfromthesestrainsinthelaboratory(datanotshown).Thelowertemperatureandilluminationledtolowertotallipids.Lipidcontentsinmicroalgaeaccumulatewhenthecellsarecultivatedunderstressconditionssuchasnutrientstress(includingnitrogenand/orphosphorusstarvation),lowlightirradiationandexposuretopHandtemperatureconditionsthataresuboptimalaswellasheavymetalsandotherchemicals(Sharmaetal.,2012).Lipidproductivityisameasureoftheamountoflipidproducedduringmicroalgaecultivation.Thelipidproductivitiesofalgalstrain4-38weresignificantlyhigherthanthoseofalgalstrainsKA2and75B1.Similarly,comparedwiththedataobtainedinthelaboratory(datanotshown),thelipidproductivitiesofthethreealgalstrainswerelower.SimilarresultswereobtainedbySforzaetal.(2012),whoreportedthatthebiomassandlipidproductivi-tiesundernaturalsunlightoutdoorswerereducedcomparedwiththedataobtainedunderartificiallightindoors.Inthisstudy,allexperimentswerecarriedoutinindoorracewaypondslitonlywithsunlight,whichreceivedlightforlessthan50%ofthetimeinagiven24-hperiod,andsomeconsumptionofbiomassbyres-pirationwouldhaveoccurredduringthenight.Thatistosay,bio-masslossduringthenightoccurred.Thiseffectofthediurnalcyclemaybecompensatedtoalargeextentbyahighaverageproductiv-ityduringdaylight(SobczukandChisti,2010).Theresultssuggestthatitwouldbeworthwhilecarryingoutfurtherstudiesofthethreestrainsunderoptimalconditionsusingthefluegasfromcoal-firedpowerplants.Thefattyacidprofilehasbeenusedasapotentialindicatorofbiodieselquality(Jietal.,2013).TheC16andC18seriescontents(aspercentagesofthetotalFAMEs)ofmicroalgaehavebeenusedtoevaluatetheoil/biodieselproductivity(Tangetal.,2011).AsshowninTable2,theC16andC18seriescontentsofthethreealgalstrainsrangedfrom40.43%to46.41%,andwerefoundtoconsistlargelyofthesaturatedfattyacid(SAFA)palmiticacid(C16:0)andthemonounsaturatedfattyacid(MUFA)palmitoleicacid(C16:1),similartotheresultsobtainedbySukeniketal.(1989)andOlofssonetal.(2012).Furthermore,fattyacidsofalgalstrain4-38suitableforbiodieselproduction,suchasmyristicacid(C14:0),palmiticacid(C16:0),palmitoleicacid(C16:1),stearicacid(C18:0),oleicacid(C18:1)andlinolenicacid(C18:2),constitutedupto48.29%ofthetotalfattyacids(TFA),whichcorrespondstoalowdegreeofunsaturationandisidealforbiodieselproduction(Xuetal.,2006;Franciscoetal.,2009).Theextentoffattyacidsaturationisknowntorespondtotem-perature(Quinnetal.,2012).Lowertemperaturesledtotheenhancementofstructurallipids(mainlypolyunsaturatedfattyacids)tofacilitatecellmembranefluidity(Tononetal.,2002).Inthisstudy,polyunsaturatedfattyacidsofthethreealgalstainsweremainlycomposedofC20:4n6(eicosadienoateacid)andC20:5n3(eicosapentaenoicacid,EPA),andaccountedfor43.90%to48.68%ofTFA,withthehighestratioforalgalstrain75B1,upto48.68%(Table2),whichcouldbeexplainedbylowercultivationtemperature.Table2alsoshowsthatalgalstrain75B1couldaccu-mulateEPAupto40.13%ofTFAundertheconditionsofthisstudy.Inaddition,theFAMEsofthethreealgalstrainswerecomposedofmorepolyunsaturatedfattyacids,whicharemoresuitableforuse58B.Zhuetal./BioresourceTechnology174(2014)53–59Table2
Fattyacidcompositionsofthethreestrains(4-38,KA2and75B1)suitableforfluegasculture.FAMEs4-38KA275B1C12:00.26±0.23a0.46±0.09a0.34±0.07aC13:00.25±0.11a0.13±0.04a0.23±0.11aC14:02.19±0.19b3.18±0.23a2.19±0.09bC14:10.12±0.01a0.15±0.01a0.42±0.47aC15:00.22±0.02ab0.22±0.02b0.19±0.01aC15:10.32±0.13a0.40±0.07a0.34±0.07aC16:015.92±0.38a15.10±1.69a13.88±0.23aC16:124.3±0.43b23.00±1.82b20.05±0.47aC17:00.21±0.04a0.18±0.04a0.17±0.01aC17:10.59±0.29a0.741±0.03a0.77±0.07aC18:00.22±0.00a0.19±0.07a0.18±0.02aC18:1n9C+t3.12±0.04b2.66±0.18a3.11±0.03bC18:2n6C+t2.54±0.03b2.23±0.14a2.81±0.017cC18:3n60.31±0.00a0.39±0.05b0.41±0.02bC20:21.00±0.08a0.92±0.08a1.02±0.13aC20:3n6+C21:03.12±0.24a2.81±0.34a3.95±0.10bC20:4n68.32±0.11b6.33±0.47a8.55±0.39bC20:3n30.35±0.35b0.06±0.10a0.00±0.00aC20:5n335.58±0.63a38.78±2.49b40.13±0.28bC22:20.46±0.22a0.64±0.28a0.41±0.12aC16:0/C20:50.45±0.005b0.39±0.07ab0.35±0.003aC16:0/C16:10.67±0.006a0.66±0.02a0.69±0.03aTotalC1640.21±0.80b38.09±3.50b33.93±0.32aTotalC186.20±0.06a5.47±0.15ab6.50±0.14bTotalC2048.33±0.50a48.89±3.27a53.66±0.25aValuesinthesamerowwithdifferentsuperscriptsaresignificantlydifferent(P<0.05).Valuesaremeans±SD.incoldweatherenvironmentsduetotheirtypicallylowergelpoint(Belarbietal.,2000).However,polyunsaturatedfattyacidspro-ducebiodieselwithgoodcold-flowpropertiesbutsusceptibilitytooxidation.Inthisstudy,mostofthefattyacidsintheneutrallipidfractionwereintheundesiredpolyunsaturatedform,butunderoptimalcultureconditions,especiallyincreaseddaytimetemperatureandlightintensity,thesaturatedformsoffattyacidswillpredominate(SobczukandChisti,2010).4.ConclusionsThreealgalstrains(4-38,KA2,75B1)werecultivatedsuccess-fullyusingfluegasfromcoal-firedpowerplantswithbiomassandlipidproductivitiesreportedforopenracewaypondcultures.Althoughlowerlipidproductivitieswereobtainedduetolowertemperaturesandilluminationlevels,algalstrain4-38appearstobeagoodpotentialsourcefortheproductionofbiodieselculturedwithfluegasbecauseofitshighTAGcontentandfattyacidcompo-sition,whicharesuitableforbiodiesel.Furthermore,biomassandlipidproductivitieswouldincreasesignificantlyunderoptimalcul-tureconditions,whichisanattractiveoptionintermsofreducingenergyconsumptionandproductioncosts.AcknowledgementsTheauthorsthankMrXiangquanZengforhishelpintheearlyphaseofthisstudyandtwoanonymousreviewersfortheirvaluablecomments.ThisworkwassupportedbytheMajorStateBasicResearchDevelopmentProgramofChina(973Program)(2011CB200901,2011CB200904)andtheNationalTechnicalSupportingProjectFoundation(2011BAD14B01)andtheNationalHighTechnologyResearchandDevelopmentProgramofChina(863Program)(2013AA065801)andGrantNo.GHME2011SW03.ReferencesAmaro,H.M.,Guedes,A.C.,Malcata,F.X.,2011.Advancesandperspectivesinusingmicroalgaetoproducebiodiesel.Appl.Energy88,3402–3410.Bligh,E.G.,Dyer,W.J.,1959.Arapidmethodoftotallipidextractionandpurification.Can.J.Biochem.Phys.37,911–917.Belarbi,E.H.,Molina,E.,Chisti,Y.,2000.Aprocessforhighyieldandscaleablerecoveryofhighpurityeicosapentaenoicacidestersfrommicroalgaeandfishoil.EnzymeMicrob.Technol.26,516–529.Brennan,L.,Owende,P.,2010.Biofuelsfrommicroalgae–areviewoftechnologiesforproduction,processing,andextractionsofbiofuelsandco-products.Renew.Sust.EnergyRev.14,557–577.Chisti,Y.,2007.Biodieselfrommicroalgae.Biotechnol.Adv.25,294–306.Chisti,Y.,2008.Biodieselfrommicroalgaebeatsbioethanol.TrendsBiotechnol.26,126–131.Converti,A.,Casazza,A.A.,Ortiz,E.Y.,Perego,P.,Borghi,M.D.,2009.EffectoftemperatureandnitrogenconcentrationonthegrowthandlipidcontentofNannochloropsisoculataandChlorellavulgarisforbiodieselproduction.Chem.Eng.Process.48,1146–1151.Chen,Z.,Gong,Y.M.,Fang,X.T.,Hu,H.H.,2012.Scenedesmussp.NJ-1isolatedfromAntarctica:asuitablerenewablelipidsourceforbiodieselproduction.WorldJ.Microbiol.Biotechnol.28,3219–3225.Doucha,J.,Straka,F.,Livansky,K.,2005.Utilizationoffluegasforcultivationofmicroalgae(Chlorellasp.)inanoutdooropenthin-layerphotobioreactor.J.Appl.Phycol.17,403–412.Douskova,I.,Doucha,J.,Livansky,K.,Machat,J.,Novak,P.,Umysova,D.,Zachleder,V.,Vitova,M.,2009.Simultaneousfluegasbioremediationandreductionofmicroalgalbiomassproductioncosts.Appl.Microbiol.Biotechnol.82,179–185.Francisco,E.,Neves,D.,Lopes,E.,Franco,T.,2009.Microalgaeasfeedstockforbiodieselproduction:carbondioxidesequestration,lipidproductionandbiofuelquality.J.Chem.Technol.Biotechnol.85,395–403.Han,F.F.,Wang,W.L.,Li,Y.G.,Shen,G.M.,Wan,M.X.,Wang,J.,2013.Changesofbiomass,lipidcontentandfattyacidscompositionunderalight–darkcycliccultureofChlorellapyrenoidosainresponsetodifferenttemperature.Bioresour.Technol.132,182–189.Jiang,L.,Luo,S.,Fan,X.,Yang,Z.,Guo,R.,2011.BiomassandlipidproductionofmarinemicroalgaeusingmunicipalwastewaterandhighconcentrationofCO2.Appl.Energy88,3336–3341.Ji,M.K.,Abou-Shanab,R.A.I.,Kim,S.H.,Salama,E.S.,Lee,S.H.,Kabra,A.N.,Lee,Y.S.,Hong,S.,Jeon,B.H.,2013.CultivationofmicroalgaespeciesintertiarymunicipalwastewatersupplementedwithCO2fornutrientremovalandbiomassproduction.Ecol.Eng.58,142–148.Lepage,G.,Roy,C.C.,1984.Improvedrecoveryoffattyacidthroughdirecttransesterificationwi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