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Biogeosciences,17,1169–1180,2020https://doi.
org/10.
5194/bg-17-1169-2020Author(s)2020.
ThisworkisdistributedundertheCreativeCommonsAttribution4.
0License.
LightavailabilitymodulatestheeffectsofwarminginamarineN2xerXiangqiYi1,Fei-XueFu2,DavidA.
Hutchins2,andKunshanGao1,31StateKeyLaboratoryofMarineEnvironmentalScience,CollegeofOceanandEarthSciences,XiamenUniversity,Xiamen361102,China2DepartmentofBiologicalSciences,UniversityofSouthernCalifornia,LosAngeles,CA90089,USA3Co-InnovationCenterofJiangsuMarineBio-industryTechnology,JiangsuOceanUniversity,Lianyungang22200,ChinaCorrespondence:KunshanGao(ksgao@xmu.
edu.
cn)Received:25September2019–Discussionstarted:30September2019Revised:23January2020–Accepted:1February2020–Published:28February2020Abstract.
Trichodesmiumspecies,asagroupofphoto-syntheticN2xers(diazotrophs),playanimportantroleinthemarinebiogeochemicalcyclesofnitrogenandcar-bon,especiallyinoligotrophicwaters.
HowongoingoceanwarmingmayinteractwithlightavailabilitytoaffectTri-chodesmiumisnotyetclear.
WegrewTrichodesmiumery-thraeumIMS101atthreetemperaturelevelsof23,27,and31Cundergrowth-limitingandgrowth-saturatinglightlev-elsof50and160molquantam2s1,respectively,foratleast10generationsandthenmeasuredphysiologicalperfor-mance,includingthespecicgrowthrate,N2xationrate,andphotosynthesis.
Lightavailabilitysignicantlymodu-latedthegrowthresponseofTrichodesmiumtotemperature,withthespecicgrowthratepeakingat27Cunderthelight-saturatingconditions,whilegrowthoflight-limitedcul-tureswasnon-responsiveacrossthetestedtemperatures(23,27,and31C).
Short-termthermalresponsesforN2xationindicatedthatbothhighgrowthtemperatureandlightinten-sityincreasedtheoptimumtemperature(Topt)forN2xa-tionanddecreaseditssusceptibilitytosupra-optimaltemper-atures(deactivationenergy–Eh).
Simultaneously,alllight-limitedcultureswithlowToptandhighEhwereunabletosustainN2xationduringshort-termexposuretohightem-peratures(33–34C)thatarenotlethalforthecellsgrownunderlight-saturatingconditions.
OurresultsimplythatTri-chodesmiumspp.
growingunderlowlightlevelswhiledis-tributeddeepintheeuphoticzoneorundercloudyweatherconditionsmightbelesssensitivetolong-termtemperaturechangesthatoccuronthetimescaleofmultiplegenerationsbutaremoresusceptibletoabrupt(lessthanonegenerationtimespan)temperaturechanges,suchasthoseinducedbycyclonesandheatwaves.
1IntroductionInvastareasoftheocean,primaryproductionisusuallylimitedbyavailabilityofnitrogen(Mooreetal.
,2013).
Inadditiontorecyclingwithintheeuphoticzone,biologicallyavailablenitrogensourcescanbesuppliedtophytoplank-tonfromupwelling,aerosoldeposition,andN2xationbydiazotrophicprokaryotes,supportingnewprimaryproduc-tion(DugdaleandGoering,1967).
Trichodesmiumisoneofthemajordiazotrophicorganismsoccurringinthepelagicoceans(Zehr,2011).
Trichodesmiumisagenusoflamen-touscyanobacteriathatexistsasbothsinglelamentsandcoloniesconsistingoftenstohundredsoftrichomesandthatisbroadlydistributedinoligotrophictropicalandsubtropicaloceans(Caponeetal.
,1997).
Itscontributiontolocalnewproductioncanevenbemoreimportantthanthatofnitratediffusioninsomeregions(Caponeetal.
,2005;LaRocheandBreitbarth,2005;Mahaffeyetal.
,2005),anditthusplaysasignicantroleinmarineecosystemsandbiogeochemi-calcyclesofnitrogenandcarbon(Sohmetal.
,2011;Zehr,2011).
Trichodesmiumhasattractedtremendousresearchinterestsinceitsdiscoveryasadiazotrophintheearly1960s(Dug-daleetal.
,1961,1964).
Recently,considerableresearchat-PublishedbyCopernicusPublicationsonbehalfoftheEuropeanGeosciencesUnion.
1170X.
Yietal.
:Lightavailabilitymodulatestheeffectsofwarmingtentionhasbeenfocusedonevaluatingeffectsoftheongoingoceanclimatechange,includingseasurfacewarmingassoci-atedwithglobalwarming,onthiskeystoneorganism(Fuetal.
,2014;HutchinsandFu,2017;Jiangetal.
,2018;Hutchinsetal.
,2007).
TheIPCCRCP8.
5scenariopredictsthatupper-oceantemperaturewillincreasebyabout3Conaveragebytheendofthe21stcentury,andthestrongestoceanwarm-ingwillhappenintropicalandsubtropicalregions(Collinsetal.
,2013).
Becauseofitsimportantroleinmarinebiogeo-chemicalcyclesandmarineecosystems,understandingtheresponsesofTrichodesmiumtooceanwarmingandtheirun-derlyingmechanismswillbecriticaltoevaluatingthepoten-tialimplicationsofclimatechangeonmarineprimarypro-ductivity,foodwebdynamics,andbiogeochemicalcycles.
Previousstudiesdemonstratethatwithoutresourcelimi-tationthegrowth-versus-temperaturecurveisunimodalinTrichodesmium,withloweranduppertolerancelimitssep-aratelyat18–20and32–34Candoptimumtemperatureat26–28C(Breitbarthetal.
,2007;ChappellandWebb,2010;Fuetal.
,2014).
Basedonthesendingsandthespatialhet-erogeneityofpresenttemperaturesandprojectedwarmingofTrichodesmium'shabitat(Caponeetal.
,1997;Collinsetal.
,2013),theeffectsofoceanwarmingonTrichodesmiumcanbespatiallydiverse,generallybenetingthoseoccurringinrelativelyhighlatitudesbutbeingharmfultothoseoccur-ringneartotheEquator(Breitbarthetal.
,2007;Fuetal.
,2014;Thomasetal.
,2012).
However,thispatterncanbedis-tortedandcomplicatedbyresourcelimitations.
Forexam-ple,itisshownthatironlimitation,whichiscommonlyex-periencedbyTrichodesmiuminnature(HutchinsandBoyd,2016;Sohmetal.
,2011),substantiallyincreasestheopti-mumtemperatureinTrichodesmium(Jiangetal.
,2018).
Similartoironavailability,lightisalsoamongthekeyenvironmentaldriversforTrichodesmium(Breitbarthetal.
,2008;CaiandGao,2015;Caietal.
,2015).
Trichodesmiumcanbedistributedfromtheseasurfacedownto150mdepth,wherelightintensityatnoonrangesfrom>2000to0.
05forallthreecompar-isons).
Overall,N2xationratesatthegrowthtemperature(Ngrowth;Fig.
1b)weresignicantlyhigherinculturesgrownunderhighlightintensitycomparedtothosegrownunderlowlightintensity(two-wayANOVA,F1,12=149.
9,P<0.
001).
Also,thegrowthtemperaturesigni-cantlyaffectedNgrowth(two-wayANOVA,F1,12=3912.
3,P<0.
001).
Differentthermaleffectsbetweenlight-saturatedandlight-limitedculturesindicatedasignicantinterac-tionbetweenlightandtemperatureinNgrowth(two-wayANOVA,F2,12=112.
7,P<0.
001).
Forlight-saturatedcul-tures,theNgrowthpeakedat27C,withavalueof17.
1±0.
5molN2mgChla1h1(±SD),whichwashigherby39%and17%thanthoseat23C(Tukey'stestcom-paringNgrowthbetweenlight-saturatedculturesgrownat27and23C,P<0.
001)and31C(Tukey'stestcom-www.
biogeosciences.
net/17/1169/2020/Biogeosciences,17,1169–1180,20201174X.
Yietal.
:LightavailabilitymodulatestheeffectsofwarmingTable1.
Resultsoftwo-wayANOVAforspecicgrowthrate,N2xationrate,effectivequantumyield,andparametersderivedfromrETRlightcurvewithinteractionsbetweentemperatureandlight.
SeeTableS2forresultsofpairwisecomparisons.
ParameterEffectdegreeoffreedom(d.
f.
)FvaluePvalueSpecicgrowthrateTemperature2,1222.
0<0.
001Light1,12662.
7<0.
001Temperature*light2,1218.
0<0.
001N2xationrate(Ngrowth)Temperature2,123912.
3<0.
001Light1,12149.
9<0.
001Temperature*light2,12112.
7<0.
001EffectivequantumyieldTemperature2,1222.
1<0.
001Light1,12233.
2<0.
001Temperature*light2,121.
80.
211rETRlightcurve:αTemperature2,1224.
5<0.
001Light1,1210.
6<0.
01Temperature*light2,120.
20.
815rETRlightcurve:EkTemperature2,125.
0<0.
05Light1,126.
0<0.
05Temperature*light2,121.
00.
394rETRlightcurve:rETRmaxTemperature2,1231.
2<0.
001Light1,12139.
8<0.
001Temperature*light2,128.
1<0.
01paringNgrowthbetweenlight-saturatedculturesgrownat27and23C,P<0.
001),respectively.
However,forlight-limitedcultures,thevalueofNgrowthat27C(6.
8±0.
2molN2mgChla1h1,±SD)wassimilartothatat23C(6.
3±0.
1molN2mgChla1h1,±SD;Tukey'stestcomparingNgrowthbetweenlight-limitedculturesgrownat27and23C,P=0.
54)butsignicantlyhigherthanthatat31C(3.
8±0.
4molN2mgChla1h1,±SD;Tukey'stestcomparingNgrowthbetweenlight-limitedculturesgrownat27and31C,P<0.
001).
3.
2PSIIeffectivequantumyield(PSII)andrETRlightresponsecurvesComparedtolight-saturatedcells,light-limitedcellshadhighervaluesofPSII(Fig.
1c;two-wayANOVA,F1,12=233.
2,P<0.
001).
Meanwhile,underbothlightregimes,PSIIinTrichodesmiumculturesgrownat31Cwassignif-icantlyhigherthanthatinculturesgrownat23and27C(two-wayANOVA,F2,12=22.
1,P<0.
001).
NointeractionbetweengrowthlightintensityandtemperatureinPSIIwasfound(two-wayANOVA,F2,12=1.
8,P=0.
211).
TherETRlightresponsecurveofTrichodesmiumIMS101wasinuencedbygrowthtemperatureinbothlight-saturated(Fig.
2a)andlight-limited(Fig.
2b)treatments.
Thisther-malimpactwasmainlyreectedintherETRmax(two-wayANOVA,F2,12=31.
2,P<0.
001),whichtendedtobehigherinculturesacclimatedto31Cthanthoseincul-turesacclimatedto23Cor27C(Table2;Fig.
2).
Addi-tionally,highgrowthlightintensitytendedtodecreasedtherETRmax(two-wayANOVA,F1,12=31.
2,P<0.
001),espe-ciallyforculturesgrownat27C(Tukey'stestcomparingrETRmaxbetweenlight-saturatedandlight-limitedculturesgrownat27C,P<0.
001).
Bothhighlightintensity(two-wayANOVA,F1,12=6.
0,P<0.
05)andhightemperatures(two-wayANOVA,F2,12=5.
0,P<0.
05)signicantlyin-creasedtheEk(Table2).
3.
3Short-termthermalresponseforN2xationOptimumtemperature(Topt)forN2xationinTri-chodesmiumIMS101wasaffectedbybothgrowthtemper-atureandlightintensity(Table3).
Generally,ToptforN2xationinlight-saturatedcultureswashigherthanthatinlight-limitedcultures,whereaswarmingeffectsonN2x-ationToptdifferedbetweenlight-saturatedandlight-limitedcultures.
Forlight-saturatedcultures,elevationsofthegrowthtemperatureraisedtheToptforN2xation.
A4Cwarm-ingwasaccompaniedbya0.
5–0.
8CincreaseinTopt,whichwas28.
7±0.
2C(±SEM,standarderrorofthemean),29.
5±0.
2C(±SEM),and30.
0±0.
3C(±SEM)forthecellsgrownat23,27,and31C,respectively.
Underlight-limitinglevels,Toptinculturesgrownat27C(Topt=28.
6±0.
2C,±SEM)washigherthanthatinculturesgrownat23C(Topt=28.
2±0.
2C,±SEM),butToptinculturesgrownat31C(Topt=27.
8±0.
2C,±SEM)wasthelow-estamongalltreatments.
Asexpected,themaximalN2x-ationrate(Nmax)inlight-saturatedcultureswashigherthanBiogeosciences,17,1169–1180,2020www.
biogeosciences.
net/17/1169/2020/X.
Yietal.
:Lightavailabilitymodulatestheeffectsofwarming1175Table2.
Thelight-harvestingefciency(α),relativeelectiontransportratemaximum(rETRmax),andlightsaturationpoint(Ek),de-rivedfromthelightcurves(Fig.
2),forTrichodesmiumgrownatdifferenttemperatureandlightintensitylevels.
Valuesrepresentthemean±standarddeviationofbiologicalreplicates(n=3).
Superscriptswithdifferentlettersrepresentsignicantdifference(Turkey'stest;moredetailsinTableS2;p<0.
05)amongthetreatments.
TheunitsofEkandrETRmaxaremicromolesofquantapersquaremeterpersecondandarbitraryunit,respectively.
GrowthconditionsLight-saturatingLight-limiting23C27C31C23C27C31Cα0.
25±0.
01ac0.
24±0.
03a0.
28±0.
01c0.
30±0.
03bc0.
28±0.
03b0.
35±0.
03bEk316±22ab322±45ab371±16a270±17b319±38ab329±21abrETRmax78±3a72±3a105±2b80±6a90±2c115±4bFigure4.
ThecombinedeffectsoftemperatureandlightintensityonthespecicgrowthrateinTrichodesmiumIMS101,withdatafromtheliteratureinvolvingatleasttwogrowthtemperaturesandthisstudy.
thatinlight-limitedcultures(Table3).
Thetemperatureef-fectonNmaxwasalsodependentonthelightavailabil-ity.
Light-saturatedNmaxwashighestinculturesgrownat27C(Nmax=19.
3±0.
4molN2mgChla1h1,±SEM),beinghigherby21%and32%thanthosegrownat23C(Nmax=16.
0±0.
3molN2mgChla1h1,±SEM)and31C(Nmax=14.
6±0.
4molN2mgChla1h1,±SEM),respectively.
However,Nmaxforlight-limitedcultureswassimilaramongdifferenttemperaturetreatments(Table3).
Thevalueofdeactivationenergy(Eh)forN2xation,re-ectingthethermalsusceptibilitytosupra-optimaltempera-tures,wasaffectedbybothlightavailabilityandgrowthtem-peraturebutnotbytheirinteraction(Table3).
EhtendedtobelowerinTrichodesmiumculturesgrownunderhightemperaturesandhighlightintensity.
WiththehighestTopt(30.
0±0.
3C,±SEM)andthelowestEh(1.
47±0.
14eV,±SEM)amongalltreatments,light-saturatedculturesac-climatedto31Cweretheonlyculturesthatcouldmain-tainconsiderableN2xationratesatassaytemperaturesashighas34C(Fig.
3).
Inaddition,bothlightavailabilityandgrowthtemperatureaffectedthedeactivationtempera-ture(Th)forN2xationinTrichodesmium,andnointeractionbetweenthesetwodriverswasfoundonTh(Table3).
Thinlight-saturatedculturestendedtobehigherthanthatinlight-limitedculturesregardlessofthegrowthtemperature.
Thwaslowerinculturesgrownat31Ccomparedtothatinculturesgrownat23or27Cunderbothlightlevels.
Theactivationenergy(Ea)forN2xationwasaffectedbygrowthtempera-turebutnotbygrowthlightintensity(Table3).
ThevaluesofEaforN2xationincreasedfrom0.
49±0.
04eV(±SEM)to0.
91±0.
05(±SEM)and1.
07±0.
04eV(±SEM)asgrowthtemperaturesincreasedfrom23to27and31C.
4DiscussionInthisstudy,lightavailabilitynotonlyaffectedgrowthrateandN2xationdirectlybutalsomodulatedtheirresponsestotemperaturechangesinTrichodesmiumIMS101.
Reducedenergysupplyduetolightlimitationleadstolowerednitro-genxationandthusreducedgrowthinthediazotroph.
Thespecicgrowthratewasmaximalat27Cforcellsgrownundersaturatinglightbutwasvirtuallyinsensitivetotem-peraturechangesacrossthetestedtemperature(23,27,and31C)forlight-limitedcultures.
TheinteractionsbetweentemperatureandlightonTri-chodesmiumdemonstratedinthisworkarerelevanttonaturallightandtemperaturevariationsandtoTrichodesmiumglobalchangephysiologyandbiogeography.
Lightsuppliesenergyforphotosynthesis,growth,andotherkeyactivities,suchasN2xationincyanobacterialdiazotrophs.
Theobservedphe-nomenonthatthegrowthratebecomeslesssensitivetotem-peraturechanges(Figs.
1aand4)inTrichodesmiumIMS101underlight-limitinglevelscanbeattributedtoinsufcienten-ergysupplyforthecellstorespondtotemperaturechanges.
www.
biogeosciences.
net/17/1169/2020/Biogeosciences,17,1169–1180,20201176X.
Yietal.
:LightavailabilitymodulatestheeffectsofwarmingTable3.
ModelparametersofthermalresponsesforN2xation.
Thestructureofthemodel'sxedeffectisN(TC)temperature*light.
Eatemperature.
Ehlight+temperature.
Thlight+temperatureinwhich"+"and""representadditiveandinteractiveeffects,re-spectively.
ParameterLightTemperature(C)EstimateSEMCI(95%)N(Tc)Light-saturated2338.
31.
0[36.
4,40.
3](molN2mgChla1h1)2739.
11.
0[37.
1,41.
1]3141.
31.
5[38.
2,44.
3]Light-limited2319.
50.
8[18.
0,21.
1]2715.
00.
8[13.
4,16.
6]3120.
31.
1[18.
2,22.
5]Ea(eV)Nolighteffect230.
490.
04[0.
41,0.
57]270.
910.
05[0.
80,1.
01]311.
070.
04[0.
98,1.
16]Eh(eV)Light-saturated234.
490.
51[3.
47,5.
51]273.
990.
31[3.
36,4.
61]311.
470.
14[1.
18,1.
75]Light-limited237.
510.
68[6.
15,8.
87]277.
010.
60[5.
82,8.
21]314.
490.
49[3.
50,5.
48]Th(C)Light-saturated2332.
60.
1[32.
3,32.
9]2732.
40.
2[32.
1,32.
8]3131.
80.
2[31.
3,32.
3]Light-limited2331.
10.
1[30.
9,31.
4]2731.
00.
1[30.
7,31.
2]3130.
30.
2[29.
9,30.
6]Topt(C)Light-saturated2328.
70.
2[28.
2,29.
1]2729.
50.
2[29.
2,29.
8]3130.
00.
3[29.
5,30.
6]Light-limited2328.
20.
2[27.
9,28.
6]2728.
60.
2[28.
3,28.
9]3127.
80.
2[27.
4,28.
2]NmaxLight-saturated2316.
00.
3[15.
3,16.
6](molN2mgChla1h1)2719.
30.
4[18.
5,20.
1]3114.
60.
4[13.
9,15.
4]Light-limited238.
30.
3[7.
6,8.
9]277.
40.
4[6.
6,8.
2]318.
60.
4[7.
8,9.
4]Whilethermalbiologicalresponsesaremainlybasedonen-zymaticperformance,lightlimitationsuppressessynthesesofenzymes(RavenandGeider,1988)andthussubsequentlylimitsthermalresponses.
Althoughlight-limitedphytoplank-toncellstypicallyallocatemoreresourcestolight-harvestingsystemstocompensateforlightshortages,atverylowir-radiancesthiscompensationcannotpreventlight-harvestingcapacityfrombeingalimitingfactorforenzymesynthesisandgrowth(RavenandGeider,1988).
FieldinvestigationsshowthatverticaldistributionsofTrichodesmiumcanreachdepthsgreaterthan100m,wherelightisabsolutelylimit-ingandtemperatureislowercomparedtosurfacetempera-ture(Olsonetal.
,2015;Roucoetal.
,2016).
Accordingtothetypicalvaluesofsurfacesolarirradiancesandtheverticalextinctioncoefcientintropicalandsubtropicaloceans(Ol-sonetal.
,2015),thedailylightdosereceivedbythelight-limitedculturesinourstudycorrespondstothatreceivedbyTrichodesmiumatadepthof50–60m.
ThecontributionofbiomassandN2xationbyTrichodesmiumatdepthsgreaterthan50mmightrangefrom7%to28%(DavisandMcGillicuddy,2006;Olsonetal.
,2015).
Therefore,theevaluationofpotentialwarmingeffectsonTrichodesmiumshouldnotbeconstrainedtothepopulationsinhabitinglight-saturatedenvironments(uppertensofmeters;BreitbarthetBiogeosciences,17,1169–1180,2020www.
biogeosciences.
net/17/1169/2020/X.
Yietal.
:Lightavailabilitymodulatestheeffectsofwarming1177al.
,2007;Jiangetal.
,2018),making3-Dmodelsindispens-able.
Inexisting3-DmodelstudiesinvolvingTrichodesmium(BoydandDoney,2002;Mooreetal.
,2002),thecombinedeffectsoftemperatureandlightonTrichodesmiumbiolog-icalactivitiesaresimplyassumedtobeadditive,whichisproventobeinappropriateinthiswork.
WhiletheabsolutevaluesoftheN2xationrateunderlight-limitingandlight-saturatinglevelscannotbedirectlycomparedonthebasisofChlacontent,sincelowerlightlevelsresultedinmorecel-lularChlacontent(Fig.
S1b),comparisonofthethermalre-sponsepatternscangenerateusefulinformationforimprov-ingmodelpredictionsofdiazotrophicresponsestooceancli-matechange.
Thermalresponsesfororganismsareknowntobeuse-fulinevaluatingthermalacclimationpotentialandprobinglowandhightemperaturetolerances(Gundersonetal,2010;Somero,2010;WayandYamori,2014).
Inthiswork,theshapeoftheshort-termthermalresponsecurvesforN2x-ationisnormalization-independentbecausecellswereex-posedtodifferentassaytemperaturesforonly1h,hardlychangingtheelementalstoichiometryorcellularpigmentcomponent.
Whenexposedtoabrupttemperaturegradients,thelight-saturatedcellsacclimatedtohighertemperaturesexhibitedhigherToptvalues(Table3)andlowerthermalsus-ceptibilitytosupra-optimaltemperatures(Eh;Table3).
Thisindicatesanincreasedcapabilityforthediazotrophtotolerateshort-termwarmingimpacts.
However,lightlimitationmadethecellsmoresusceptibletowarmingduetodecreasedToptandincreasedEhforN2xation(Table3).
Moreover,withlightlimitation,acclimationtohightemperaturesdidnothelpTrichodesmiumcellstolerateshort-termsupra-optimaltem-peratures.
Ontheotherhand,ChlauorescencedatashowthatthePSIIinlight-limitedcultureswasashealthyasthatincellsgrownundersaturatinglight(Fig.
1c,2),andithasbeenshownthatdamagetoPSIIusuallyoccursattemperaturesabove45C(Yamorietal.
,2014).
Therefore,thecollapseofN2xationathightemperatureswasnotlikelycausedbythedysfunctionofthephotosystemsbutmightbecausedbytheuncouplingofadenosinetriphosphate(ATP)synthesistoelectrontransport,sinceprotonleakinessofthethylakoidmembranehasbeenfrequentlyproposedasaproblemathightemperatures(Yamorietal.
,2014).
Thisisconsistentwiththeobservationthatsupra-optimaltemperatureinhibitionofN2xationwasaggravatedbylightlimitation(Fig.
3).
Inaddi-tion,damagetonitrogenaseathightemperaturesmightalsobeoneofthereasonsresponsibleforthefasterdropofN2x-ationathightemperaturesinlight-limitedcultures(Galloneta.
,1993).
Thisisbecausetheextrainvestmentofresourcestorepairdamagednitrogenasecouldnotbesupportedunderlight-limitingconditions(Fig.
3b).
Therefore,lightavailabil-ityexertscriticalcontrolontheacclimationpotentialofN2xationinTrichodesmiumtowarming.
Acclimationtodifferenttemperaturesalsoaffectedtheactivationenergy(Ea)forN2xationinTrichodesmiumIMS101(Table3).
ForTrichodesmiumspecies,N2xationcanbecontrolledbysupplyofATPandreducingequivalents,mainlycomingfromphotosynthesis,andtheinherentcat-alyticcapacityofthenitrogenase.
Thesetwoprocessesmayexhibitdifferenttemperaturedependence,i.
e.
,differentEa.
TheEaofthecontrollingprocessdeterminestheN2xationEa(Hikosakaetal.
,2006;Staaletal.
,2003).
Therefore,thedifferencesinN2xationEabetweenculturesgrownatdif-ferenttemperaturesmayreectthatN2xationwasprimar-ilycontrolledbydifferentprocessesinculturesacclimatedtodifferenttemperatures.
Preliminaryevidencesupportingthishypothesiscamefromthevariouseffectsofassaylightinten-sityonthevaluesofEaforN2xationbetweenlight-limitedculturesgrownat23and27C(TableS1;Fig.
S2).
ForTri-chodesmiumgrownunderlight-limitinglevels,thelowerEavaluesinculturesacclimatedto23Cweresignicantlyele-vatedbytheincreasedassaylightintensitywhichcanprovidemoreATPandreducingequivalents(TableS1;Fig.
S2a).
ThissuggeststhattheconstraintshouldbethesupplyofATPandreducingequivalents.
ThehigherEavaluesinculturesacclimatedto27Cwereinsensitivetotheassaylightinten-sitychanges,suggestingthatN2xationshouldnotbecon-trolledbythesupplyofATPandreducingequivalentsatthisoptimaltemperaturebutmaypossiblybecontrolledbyinher-entcatalyticcapacityofthenitrogenase(TableS1;Fig.
S2b).
Theshort-termthermalresponsesforN2xationmirrorthermalshockresponses.
Ifcellsareexposedtothethermalchangesforlongertime,acclimationwilldenitelychangethethermalresponsesforN2xationinTrichodesmium(Bre-itbarthetal.
,2007;Fuetal.
,2014;Staaletal.
,2003).
Tocomparetheshort-termandacclimatedthermalresponsesforN2xation,wecalculatedthecorrespondingvaluesofEa,Eh,andTopt,whichare,respectively,0.
93±0.
64eV(±SEM),1.
86±1.
19eV(±SEM),and27.
1±1.
0C(±SEM)forfullyacclimatedN2xationwithintherangeof20–34CgrowthtemperaturesinTrichodesmiumIMS101(Breitbarthetal.
,2007).
ThesevaluesofEaandEharecomparabletothosederivedfromshort-termthermalresponseforN2x-ationinthesamestraingrownunderlight-saturatingcon-ditionsand31Cinourstudy(Table3),buttheToptvalueislowerthanthatfromshort-termthermalresponse.
Ontheotherhand,wetriedtoderivevaluesofEa,Eh,andToptforacclimatedN2xationratesinanotherthreeTrichodesmiumerythraeumstrains(strainsRLI,KO4-20,and21-75;Fuetal.
,2014),butthemodelttingfailedtoconverge.
Insteadofbeennegativelyskewed,thethermalresponsecurvesofac-climatedN2xationinthesethreeTrichodesmiumstrainsarenearlysymmetrical.
ThesecomparisonsshowthatthermalresponseforN2xationinTrichodesmiumisstrain-specicandisaffectedonthetimescaleofacclimationprocess.
Intheoceans,Trichodesmiumandotherpelagicphyto-planktonareoftenexposedtoabrupttemperaturechangesduetostronglydisturbedweatherconditions,suchastrop-icalcyclonesandmarineheatwaves.
Globalwarminghasbeenpredictedtoincreasebothtropicalcycloneintensitiesandthefrequencyofthemostintensetropicalcyclones(El-www.
biogeosciences.
net/17/1169/2020/Biogeosciences,17,1169–1180,20201178X.
Yietal.
:Lightavailabilitymodulatestheeffectsofwarmingsneretal.
,2008;Knutsonetal.
,2010;Wehneretal.
,2018).
Upper-oceantemperaturedeclinespriortoandduringacy-cloneeventandthenincreasesabruptlyafterwards(Lietal.
,2009),accompaniedbystrongvariationsinsurfacesolarra-diationandstratication(SriverandHuber,2007).
Theseabrupttemperaturechangesoccurringinnaturearenotasacuteasthoseinourexperiment.
Forexample,temperaturechangescausedbycyclonesandheatwavesareontheorderof0.
5–1Cperday(Babinetal.
,2004;Beca-Carreteroetal.
,2018).
Nonetheless,thesetemperaturechangesoccurwithinonegenerationofTrichodesmiumbecauseofitslowgrowthrate,notleavingenoughtimeforfullacclimation.
Therefore,thevaluesofEa,Eh,Th,andToptprovidedinthisstudycanlikelyserveasproxiesforsometypesofabruptnaturaltem-peratureincreases.
Dataavailability.
Thedataareavailableuponrequesttothecorre-spondingauthor(KunshanGao).
Supplement.
Thesupplementrelatedtothisarticleisavailableon-lineat:https://doi.
org/10.
5194/bg-17-1169-2020-supplement.
Authorcontributions.
KGandXYdesignedtheexperiment.
XYcarriedouttheexperiment.
XY,FXF,DAH,andKGanalyzedthedataandwrotethepaper.
Competinginterests.
Theauthorsdeclarethattheyhavenoconictofinterest.
Financialsupport.
ThisresearchhasbeensupportedbytheNa-tionalKeyR&DProgramofChina(grantno.
2016YFA0601400),theNationalNaturalScienceFoundationofChina(grantnos.
41720104005and41721005),theJointProjectoftheNationalNaturalScienceFoundationofChinaandShandongProvince(grantno.
U1606404),andtheUSNationalScienceFoundation(grantnos.
OCE1538525,OCE1657757,andOCE1638804).
Reviewstatement.
ThispaperwaseditedbyCarolRobinsonandreviewedbythreeanonymousreferees.
ReferencesBabin,S.
M.
,Carton,J.
A.
,Dickey,T.
D.
,andWiggert,J.
D.
:Satelliteevidenceofhurricane-inducedphytoplanktonbloomsinanoceanicdesert,J.
Geophys.
Res.
,109,C03043,https://doi.
org/10.
1029/2003jc001938,2004.
Beca-Carretero,P.
,Guihéneuf,F.
,Marín-Guirao,L.
,Bernardeau-Esteller,J.
,García-Muoz,R.
,Stengel,D.
B.
,andRuiz,J.
M.
:EffectsofanexperimentalheatwaveonfattyacidcompositionintwoMediterraneanseagrassspecies,Mar.
Pollut.
Bull.
,134,27–37,https://doi.
org/10.
1016/j.
marpolbul.
2017.
12.
057,2018.
Boatman,T.
G.
,Lawson,T.
,andGeider,R.
J.
:Akeyma-rinediazotrophinachangingocean:Theinteractingef-fectsoftemperature,CO2andlightonthegrowthofTri-chodesmiumErythraeumims101,PLOSONE,12,e0168796,https://doi.
org/10.
1371/journal.
pone.
0168796,2017.
Boyd,P.
W.
,andDoney,S.
C.
:Modellingregionalresponsesbyma-rinepelagicecosystemstoglobalclimatechange,Geophys.
Res.
Lett.
,29,53-1–53-4,https://doi.
org/10.
1029/2001GL014130,2002.
Breitbarth,E.
,Oschlies,A.
,andLaRoche,J.
:Physiologicalcon-straintsontheglobaldistributionofTrichodesmium–ef-fectoftemperatureondiazotrophy,Biogeosciences,4,53–61,https://doi.
org/10.
5194/bg-4-53-2007,2007.
Breitbarth,E.
,Wohlers,J.
,Kls,J.
,LaRoche,J.
,andPeeken,I.
:NitrogenxationandgrowthratesofTrichodesmiumIMS-101asafunctionoflightintensity,Mar.
Ecol.
Prog.
Ser.
,359,25–36,https://doi.
org/10.
3354/meps07241,2008.
Cai,X.
andGao,K.
:Levelsofdailylightdosesunderchangedday-nightcyclesregulatetemporalsegregationofphotosynthesisandN2xationinthecyanobacteriumTri-chodesmiumerythraeumIMS101,PLOSONE,10,e0135401,https://doi.
org/10.
1371/journal.
pone.
0135401,2015.
Cai,X.
,Gao,K.
,Fu,F.
,Campbell,D.
,Beardall,J.
,andHutchins,D.
:Electrontransportkineticsinthediazotrophiccyanobac-teriumTrichodesmiumspp.
grownacrossarangeoflightlevels,Photosynth.
Res.
,124,45–56,https://doi.
org/10.
1007/s11120-015-0081-5,2015.
Capone,D.
G.
:Determinationofnitrogenaseactivityinaquaticsamplesusingtheacetylenereductionprocedure,in:CurrentMethodsinAquaticMicrobiology,editedby:Kemp,P.
F.
,Sherr,B.
F.
,Sherr,E.
B.
,andCole,J.
J.
,LewisPublishers,NewYork,621–631,1993.
Capone,D.
G.
,Zehr,J.
P.
,Paerl,H.
W.
,Bergman,B.
,andCarpenter,E.
J.
:Trichodesmium,agloballysignif-icantmarinecyanobacterium,Science,276,1221–1229,https://doi.
org/10.
1126/science.
276.
5316.
1221,1997.
Capone,D.
G.
,Burns,J.
A.
,Montoya,J.
P.
,Subramaniam,A.
,Mahaffey,C.
,Gunderson,T.
,Michaels,A.
F.
,andCarpen-ter,E.
J.
:NitrogenxationbyTrichodesmiumspp.
:Anim-portantsourceofnewnitrogentothetropicalandsubtropicalNorthAtlanticOcean,GlobalBiogeochem.
Cy.
,19,GB2024,https://doi.
org/10.
1029/2004GB002331,2005.
Chappell,P.
D.
andWebb,E.
A.
:AmolecularassessmentoftheironstressresponseinthetwophylogeneticcladesofTrichodesmium,Environ.
Microbiol.
,12,13–27,https://doi.
org/10.
1111/j.
1462-2920.
2009.
02026.
x,2010.
Chen,Y.
-B.
,Zehr,J.
P.
,andMellon,M.
:Growthandnitro-genxationofthediazotrophiclamentousnonheterocystouscyanobacteriumTrichodesmiumsp.
IMS101indenedme-dia:Evidenceforacircadianrhythm,J.
Phycol.
,32,916–923,https://doi.
org/10.
1111/j.
0022-3646.
1996.
00916.
x,1996.
Collins,M.
,R.
Knutti,,J.
Arblaster,J.
-L.
Dufresne,T.
Fichefet,P.
Friedlingstein,X.
Gao,W.
J.
Gutowski,T.
Johns,G.
Krinner,M.
Shongwe,C.
Tebaldi,Weaver,A.
J.
,andWehner,M.
:Long-termclimatechange:Projections,commitmentsandirreversibil-ity,ClimateChange2013:ThePhysicalScienceBasis,Contribu-tionOfWorkingGroupIToTheFifthAssessmentReportOfTheBiogeosciences,17,1169–1180,2020www.
biogeosciences.
net/17/1169/2020/X.
Yietal.
:Lightavailabilitymodulatestheeffectsofwarming1179IntergovernmentalPanelOnClimateChange,editedby:Stocker,T.
F.
,D.
Qin,G.
-K.
Plattner,M.
Tignor,S.
K.
Allen,J.
Boschung,A.
Nauels,Y.
Xia,Bex,V.
,andMidgley,P.
M.
,CambridgeUni-versityPress,Cambridge,UnitedKingdomandNewYork,NY,USA,1029–1136,2013.
Davis,C.
S.
andMcGillicuddy,D.
J.
:TransatlanticabundanceoftheN2-xingcolonialcyanobacteriumTrichodesmium,Science,312,1517–1520,https://doi.
org/10.
1126/science.
1123570,2006.
Dugdale,R.
C.
andGoering,J.
J.
:Uptakeofnewandregeneratedformsofnitrogeninprimaryproductivity,Limnol.
Oceanogr.
,12,196–206,https://doi.
org/10.
4319/lo.
1967.
12.
2.
0196,1967.
Dugdale,R.
C.
,Menzel,D.
W.
,andRyther,J.
H.
:NitrogenxationintheSargassoSea,Deep-SeaRes.
,7,297–300,https://doi.
org/10.
1016/0146-6313(61)90051-X,1961.
Dugdale,R.
C.
,Goering,J.
J.
,andRyther,J.
H.
:HighnitrogenxationratesintheSargassoSeaandtheArabianSea,Limnol.
Oceanogr.
,9,507–510,https://doi.
org/10.
4319/lo.
1964.
9.
4.
0507,1964.
Eilers,P.
H.
C.
andPeeters,J.
C.
H.
:Amodelfortherelationshipbetweenlightintensityandtherateofpho-tosynthesisinphytoplankton,Ecol.
Model.
,42,199–215,https://doi.
org/10.
1016/0304-3800(88)90057-9,1988.
Elsner,J.
B.
,Kossin,J.
P.
,andJagger,T.
H.
:Theincreasingin-tensityofthestrongesttropicalcyclones,Nature,455,92–95,https://doi.
org/10.
1038/nature07234,2008.
Fu,F.
X.
,Yu,E.
,Garcia,N.
S.
,Gale,J.
,Luo,Y.
,Webb,E.
A.
,andHutchins,D.
A.
:Differingresponsesofma-rineN2xerstowarmingandconsequencesforfuturedia-zotrophcommunitystructure,Aquat.
Microb.
Ecol.
,72,33–46,https://doi.
org/10.
3354/ame01683,2014.
Gallon,J.
R.
,Pederson,D.
M.
,andSmith,G.
D.
:Theef-fectoftemperatureonthesensitivityofnitrogenasetooxygeninthecyanobacteriaAnabaenacylindrica(Lemmer-mann)andGloeothece(Ngeli),NewPhytol.
,124,251–257,https://doi.
org/10.
1111/j.
1469-8137.
1993.
tb03814.
x,1993.
Garcia,N.
S.
,Fu,F.
X.
,Breene,C.
L.
,Bernhardt,P.
W.
,Mulhol-land,M.
R.
,Sohm,J.
A.
,andHutchins,D.
A.
:InteractiveeffectsofirradianceandCO2onCO2xationandN2xationinthedi-azotrophTrichodesmiumerythraeum(cyanobacteria)J.
Phycol.
,47,1292–1303,2011.
Gillooly,J.
F.
,Brown,J.
H.
,West,G.
B.
,Savage,V.
M.
,andCharnov,E.
L.
:Effectsofsizeandtemper-atureonmetabolicrate,Science,293,2248–2251,https://doi.
org/10.
1126/science.
1061967,2001.
Gunderson,C.
A.
,O'hara,K.
H.
,Campion,C.
M.
,Walker,A.
V.
,andEdwards,N.
T.
:Thermalplasticityofphoto-synthesis:theroleofacclimationinforestresponsestoawarmingclimate,Glob.
ChangeBiol.
,16,2272–2286,https://doi.
org/10.
1111/j.
1365-2486.
2009.
02090.
x,2010.
Hikosaka,K.
,Ishikawa,K.
,Borjigidai,A.
,Muller,O.
,andOn-oda,Y.
:Temperatureacclimationofphotosynthesis:mech-anismsinvolvedinthechangesintemperaturedepen-denceofphotosyntheticrate,J.
Exp.
Bot.
,57,291–302,https://doi.
org/10.
1093/jxb/erj049,2006.
Hutchins,D.
A.
andBoyd,P.
W.
:Marinephytoplanktonandthechangingoceanironcycle,Nat.
Clim.
Change,6,1072–1079,https://doi.
org/10.
1038/nclimate3147,2016.
Hutchins,D.
A.
andFu,F.
:Microorganismsandoceanglobalchange,Nat.
Microbiol.
,2,17058,https://doi.
org/10.
1038/nmicrobiol.
2017.
58,2017.
Hutchins,D.
A.
,Fu,F.
X.
,Zhang,Y.
,Warner,M.
E.
,Feng,Y.
,Portune,K.
,Bernhardt,P.
W.
,andMulholland,M.
R.
:CO2controlofTrichodesmiumN2xation,photosynthesis,growthrates,andelementalratios:Implicationsforpast,present,andfu-tureoceanbiogeochemistry,Limnol.
Oceanogr.
,52,1293–1304,https://doi.
org/10.
4319/lo.
2007.
52.
4.
1293,2007.
Hutchins,D.
A.
,Walworth,N.
G.
,Webb,E.
A.
,Saito,M.
A.
,Moran,D.
,McIlvin,M.
R.
,Gale,J.
,andFu,F.
-X.
:IrreversiblyincreasednitrogenxationinTrichodesmiumexperimentallyadaptedtoelevatedcarbondioxide,Nat.
Commun.
,6,8155,https://doi.
org/10.
1038/ncomms9155,2015.
Jiang,H.
-B.
,Fu,F.
-X.
,Rivero-Calle,S.
,Levine,N.
M.
,Saudo-Wilhelmy,S.
A.
,Qu,P.
-P.
,Wang,X.
-W.
,Pinedo-Gonzalez,P.
,Zhu,Z.
,andHutchins,D.
A.
:Oceanwarmingalleviatesironlim-itationofmarinenitrogenxation,Nat.
Clim.
Change,8,709–712,https://doi.
org/10.
1038/s41558-018-0216-8,2018.
Knutson,T.
R.
,McBride,J.
L.
,Chan,J.
,Emanuel,K.
,Holland,G.
,Landsea,C.
,Held,I.
,Kossin,J.
P.
,Srivastava,A.
K.
,andSugi,M.
:Tropicalcyclonesandclimatechange,Nat.
Geosci.
,3,157–163,https://doi.
org/10.
1038/ngeo779,2010.
LaRoche,J.
andBreitbarth,E.
:Importanceofthediazotrophsasasourceofnewnitrogenintheocean,J.
SeaRes.
,53,67–91,https://doi.
org/10.
1016/j.
seares.
2004.
05.
005,2005.
Levitan,O.
,Brown,C.
M.
,Sudhaus,S.
,Campbell,D.
,LaRoche,J.
,andBerman-Frank,I.
:RegulationofnitrogenmetabolisminthemarinediazotrophTrichodesmiumIMS101undervary-ingtemperaturesandatmosphericCO2concentrations,Envi-ron.
Microbiol.
,12,1899–1912,https://doi.
org/10.
1111/j.
1462-2920.
2010.
02195.
x,2010.
Li,F.
,Beardall,J.
,Collins,S.
,andGao,K.
:Decreasedphoto-synthesisandgrowthwithreducedrespirationinthemodeldi-atomPhaeodactylumtricornutumgrownunderelevatedCO2over1800generations,Glob.
ChangeBiol.
,23,127–137,https://doi.
org/10.
1111/gcb.
13501,2017.
Li,G.
,Wu,Y.
,andGao,K.
:EffectsofTyphoonKaemioncoastalphytoplanktonassemblagesintheSouthChinaSea,withspecialreferencetotheeffectsofsolarUVradiation,J.
Geophys.
Res.
,114,G04029,https://doi.
org/10.
1029/2008jg000896,2009.
Mahaffey,C.
,Michaels,A.
F.
,andCapone,D.
G.
:Theco-nundrumofmarineN2xation,Am.
J.
Sci.
,305,546–595,https://doi.
org/10.
2475/ajs.
305.
6-8.
546,2005.
Moore,C.
M.
,Mills,M.
M.
,Arrigo,K.
R.
,Berman-Frank,I.
,Bopp,L.
,Boyd,P.
W.
,Galbraith,E.
D.
,Geider,R.
J.
,Guieu,C.
,Jaccard,S.
L.
,Jickells,T.
D.
,LaRoche,J.
,Lenton,T.
M.
,Mahowald,N.
M.
,Maraón,E.
,Marinov,I.
,Moore,J.
K.
,Nakatsuka,T.
,Oschlies,A.
,Saito,M.
A.
,Thingstad,T.
F.
,Tsuda,A.
,andUlloa,O.
:Processesandpat-ternsofoceanicnutrientlimitation,Nat.
Geosci.
,6,701–710,https://doi.
org/10.
1038/ngeo1765,2013.
Moore,J.
K.
,Doney,S.
C.
,Kleypas,J.
A.
,Glover,D.
M.
,andFung,I.
Y.
:Anintermediatecomplexitymarineecosystemmodelfortheglobaldomain,Deep-SeaRes.
Pt.
II,49,403–462,https://doi.
org/10.
1016/S0967-0645(01)00108-4,2002.
Olson,E.
M.
,McGillicuddyJr.
,D.
J.
,Dyhrman,S.
T.
,Waterbury,J.
B.
,Davis,C.
S.
,andSolow,A.
R.
:Thedepth-distributionofnitrogenxationbyTrichodesmiumspp.
coloniesinthetropical-www.
biogeosciences.
net/17/1169/2020/Biogeosciences,17,1169–1180,20201180X.
Yietal.
:LightavailabilitymodulatestheeffectsofwarmingsubtropicalNorthAtlantic,Deep-SeaRes.
PT.
I.
,104,72–91,https://doi.
org/10.
1016/j.
dsr.
2015.
06.
012,2015.
Padeld,D.
,Yvon-Durocher,G.
,Buckling,A.
,Jennings,S.
,andYvon-Durocher,G.
:Rapidevolutionofmetabolictraitsexplainsthermaladaptationinphytoplankton,Ecol.
Lett.
,19,133–142,https://doi.
org/10.
1111/ele.
12545,2015.
Prufert-Bebout,L.
,Paerl,H.
W.
,andLassen,C.
:Growth,nitrogenxation,andspectralattenuationincultivatedTrichodesmiumspecies,Appl.
Environ.
Microbiol.
,59,1367–1375,1993.
Ralph,P.
J.
andGademann,R.
:Rapidlightcurves:Apowerfultooltoassessphotosyntheticactivity,Aquat.
Bot.
,82,222–237,https://doi.
org/10.
1016/j.
aquabot.
2005.
02.
006,2005.
Raven,J.
A.
andGeider,R.
J.
:Temperatureandalgalgrowth,NewPhytol.
,110,441–461,https://doi.
org/10.
1111/j.
1469-8137.
1988.
tb00282.
x,1988.
Ritchie,R.
J.
:ConsistentSetsofSpectrophotometricChlorophyllEquationsforAcetone,MethanolandEthanolSolvents,Pho-tosynth.
Res.
,89,27–41,https://doi.
org/10.
1007/s11120-006-9065-9,2006.
Rouco,M.
,Haley,S.
T.
,Alexander,H.
,Wilson,S.
T.
,Karl,D.
M.
,andDyhrman,S.
T.
:VariabledepthdistributionofTri-chodesmiumcladesintheNorthPacicOcean,Env.
Microbiol.
Rep.
,8,1058–1066,https://doi.
org/10.
1111/1758-2229.
12488,2016.
Schaum,C.
E.
,Buckling,A.
,Smirnoff,N.
,Studholme,D.
J.
,andYvon-Durocher,G.
:Environmentaluctuationsacceleratemolecularevolutionofthermaltoleranceinamarinediatom,Nat.
Commun.
,9,1719,https://doi.
org/10.
1038/s41467-018-03906-5,2018.
Schooleld,R.
M.
,Sharpe,P.
J.
H.
,andMagnuson,C.
E.
:Non-linearregressionofbiologicaltemperature-dependentratemod-elsbasedonabsolutereaction-ratetheory,J.
Theor.
Biol.
,88,719–731,https://doi.
org/10.
1016/0022-5193(81)90246-0,1981.
Sharpe,P.
J.
H.
andDeMichele,D.
W.
:Reactionkineticsofpoikilothermdevelopment,J.
Theor.
Biol.
,64,649–670,https://doi.
org/10.
1016/0022-5193(77)90265-X,1977.
Sohm,J.
A.
,Webb,E.
A.
,andCapone,D.
G.
:Emergingpatternsofmarinenitrogenxation,Nat.
Rev.
Microbiol.
,9,499–508,https://doi.
org/10.
1038/nrmicro2594,2011.
Somero,G.
N.
:Thephysiologyofclimatechange:howpo-tentialsforacclimatizationandgeneticadaptationwilldeter-mine"winners"and"losers",J.
Exp.
Biol.
,213,912–920,https://doi.
org/10.
1242/jeb.
037473,2010.
Sriver,R.
L.
andHuber,M.
:Observationalevidenceforanoceanheatpumpinducedbytropicalcyclones,Nature,447,577–580,https://doi.
org/10.
1038/nature05785,2007.
Staal,M.
,Meysman,F.
J.
R.
,andStal,L.
J.
:TemperatureexcludesN2-xingheterocystouscyanobacteriainthetropicaloceans,Na-ture,425,504–507,https://doi.
org/10.
1038/nature01999,2003.
Suggett,D.
J.
,LeFloc'H,E.
,Harris,G.
N.
,Leonardos,N.
,andGei-der,R.
J.
:DifferentstrategiesofphotoacclimationbytwostrainsofEmilianiahuxleyi(Haptophyta),J.
Phycol.
,43,1209–1222,https://doi.
org/10.
1111/j.
1529-8817.
2007.
00406.
x,2007.
Thomas,M.
K.
,Kremer,C.
T.
,Klausmeier,C.
A.
,andLitchman,E.
:Aglobalpatternofthermaladaptationinmarinephytoplankton,Science,338,1085–1088,https://doi.
org/10.
1126/science.
1224836,2012.
Tong,S.
,Gao,K.
,andHutchins,D.
A.
:AdaptiveevolutioninthecoccolithophoreGephyrocapsaoceanicafollowing1,000gener-ationsofselectionunderelevatedCO2,GlobalChangeBiol.
,24,3055–3064,https://doi.
org/10.
1111/gcb.
14065,2018.
Villareal,T.
andCarpenter,E.
:Buoyancyregulationandthepo-tentialforverticalmigrationintheoceaniccyanobacteriumTri-chodesmium,Microb.
Ecol.
,45,1–10,2003.
Way,D.
A.
andYamori,W.
:Thermalacclimationofphotosynthesis:ontheimportanceofadjustingourdenitionsandaccountingforthermalacclimationofrespiration,Photosynth.
Res.
,119,89–100,https://doi.
org/10.
1007/s11120-013-9873-7,2014.
Wehner,M.
F.
,Reed,K.
A.
,Loring,B.
,Stone,D.
,andKrishnan,H.
:Changesintropicalcyclonesunderstabilized1.
5and2.
0CglobalwarmingscenariosassimulatedbytheCommunityAtmo-sphericModelundertheHAPPIprotocols,EarthSyst.
Dynam.
,9,187–195,https://doi.
org/10.
5194/esd-9-187-2018,2018.
Yamori,W.
,Hikosaka,K.
,andWay,D.
A.
:TemperatureresponseofphotosynthesisinC3,C4,andCAMplants:temperatureaccli-mationandtemperatureadaptation,Photosynth.
Res.
,119,101–117,https://doi.
org/10.
1007/s11120-013-9874-6,2014.
Zehr,J.
P.
:Nitrogenxationbymarinecyanobacteria,TrendsMi-crobiol.
,19,162–173,https://doi.
org/10.
1016/j.
tim.
2010.
12.
004,2011.
Biogeosciences,17,1169–1180,2020www.
biogeosciences.
net/17/1169/2020/