PhotosynthesisResearch7 - PDF document

PhotosynthesisResearch7–10,2002.©2002KluwerAcademicPublishers.PrintedintheNetherlands.DeÞnitionofphotosynthesisHistoryofthewordphotosynthesisandevolutionofitsdeÞnitionHowardGestDepartmentofBiologyandDepartmentofHistoryandPhilosophyofScience,IndianaUniversity,BloomingtonIN47405,USA(e-mail:hgest@bio.indiana.edu) 8 Figure1.CharlesReidBarnes(1858–1910).Theabovephoto-graphwaspreparedandprovidedbyGovindjee.OriginalsourceAnonymous(1910).MacMillansuggested[evidentlywhatismeanthereisÔsuggestedapreferenceforÕ]theword‘photosynthesis’[ÞrstpoposedbyBarnesin1893asetymologicallymoresatisfactoryandaccur-ate,aclaimwhichDrBarnesshowedcouldnotbemaintained.ThesuggestionofDrBarnesnotonlyreceivedtacitacceptancebythebotanistsoftheassociation,butwaspracticallyapprovedbytheMadisonCongressinthecourseofadiscus-sionuponthispoint.Intheinterestofharmony,therefore,evenifcourtesybeignored,thewordsubstitutedforassimilation,ifanyweretobein-serted,shouldhavebeen‘photosyntax’andnot‘photosynthesis’.Itmustbenotedthat,asidefromBarnes(1893),therewerenopublisheddiscussionsofthe1893MadisonmeetingorProceedingsoftheCongressthatmention‘photosynthesis’or‘photosyntax.’Anobit-uaryofBarnes(Anonymous1910;seeFigure1)de-scribeshisdistinguishedcareerandhismanyinterestsinplantbiology.UseofthenewtermsItisawell-knownphenomenonthattheintroductionofnewscientictermsisfrequentlyresisted.Atabotanymeetingin1896,Barnes(1896)madeabriefcommentinthisconnection:...thewordphotosyntax,proposedin1893bythespeaker,butobjectedtobyProfessorMacMillanasetymologicallybad,hasbeenresubmittedtothreecompetentGreekscholarsandpronouncedbyalltobelinguisticallyunobjectionableandac-curatelyexpressiveoftheprocessofcarbohydrateformationasnowunderstood.In1898,Barnesfeltobligedtobringuptheter-minologyquestionagain,thistimeinapaperentitled‘So-called“Assimilation”,’publishedintheGermanjournalBotanischesCentralblatt(Barnes1898).Pub-licationinthisjournalisofsignicancebecauseoneoftheleadingplantphysiologistsoftheday,WilhelmPfeffer,wasGerman.Inhis1898paper,Barnesreferstohis1893paperandsays:Thisterm[i.e.,photosyntax]Ihavesinceem-ployedinlecturingandwritingandithascomeintousebyanumberofstudentsinthiscountry.AtthesametimeProfessorMacMillanoftheUni-versityofMinnesotaexpressedhispreferenceforthetermphotosynthesis,whichinthesamepaperIindicatedasanavailableword(emphasisad-ded),butrejectedasetymologicallylessaccurate.ThelattertermhasbeentakenupbyProfessorMacDougaloftheUniversityofMinnesotaandusedbyhim,bothinhistranslationofOels’sPßanzenphysiologischeVersucheandalsoinhisExperimentalPlantPhysiology.ThepropoundingofthesametermbyHansen(noinitialgiven,inapaperpublishedin1898)isofvalueonlyasatardyrecognitionofthefactthatthetermassimilationcannolongerbecorrectlyused.Itisnotimportantwhetherphotosyntaxorphotosynthesis,orsomeotherword,nallycomesintogeneralusetode-scribethemanufactureofcarbohydratesbygreentissuesundertheactionoflight.Itishightime,however,thatwedropaspromptlyaspossible,theuseofassimilationforthisoranysimilarprocess.ThereasonsforthisIhavesetforthinthepaper‘Onthefoodofgreenplants’previouslyreferredto.EventhoughBarnespreferredtheterm‘photosyn-tax,’hewasthersttopublishtheword‘photosyn-thesis’asanalternative.Historyhasshownthat,astimewenton,anincreasingnumberofinvestigatorschosetousephotosynthesis.Someauthors,however,werelaggard.Forexample,F.F.Blackmanandhis associatescontinuedtousetheterm‘vegetableas-similation’aslateas1905(BlackmanandMatthaeiPfefferÕsfailuretocreditBarnesWilhelmPfeffer(1845–1920)wasafamousplantphysiologist,amemberofmanylearnedsocietiesandtherecipientofmanyhonors.In1881,hepub-lishedamonumentalhandbookonplantphysiology:‘Panzenphysiologie:einHandbuchderLehrevomStoffwechselsundKraftwechelsinderPanze’[W.Engelmann,Leipzig].VolumeIofthesecondeditionwaspublishedin1897,VolumeIIin1904.Theau-thorindexforbothvolumesiscontainedinVolumeII,butBarnes’snameisabsent.ThesubjectindexforVolumesIandIIisalsoinVolumeII,andhasthefollowingtwoentries:‘Photosynthese,BegriffI,p.273;PhotosynthetischeKohlensäureassimilation,I,pp.284.’Again,nomentionofBarnesorofhis1893paper.Itisclear,however,thatPfefferknewthatthewordphotosynthesiswascoinedbyBarnes.SeveraleditionsofPfeffer’sfamoushandbookweretrans-latedintoEnglishandpublishedbyAlfredJ.EwartoftheBotanicalDepartment,UniversityofOxford.TheEnglisheditionof1900(Ewart1900)containsaPreface,inEnglish,writtenbyPfefferin1897.Inthisparticularedition,Ewartaddedseveralfootnotes,oneofwhichisparticularlypertinent(p.302):Theterm‘photosyntheticassimilation’isaper-fectlygeneralone,andwouldincludetheassimila-tionofothercompoundsbytheaidoflight,shouldanysuchprocessesbediscoveredinthefuture[fact,H.Molischdiscoveredthephotoheterotrophicgrowthmodeofpurplebacteriain1907].Thephotosyntheticassimilationofcarbonicacidmaybetermedcarbondioxideassimilation.‘Carbon-assimilation’isobviouslyincorrect,forinanalogywiththeterm‘nitrogenassimilation’wouldin-dicatethatcarboncouldbedirectlyassimilated.Theuncouthterm‘photosyntax’isquiteunneces-sary,andmoreoverhasbeenerroneouslyusedtoindicateallcasesofcarbondioxideassimilation,althoughtheoccurrenceofapowerofchemo-syntheticassimilationofcarbonicacidincertainbacteriawasalreadywellknown.ItisremarkableandregrettablethatneitherthefootnotenorthebookcitesBarnesorhis1893paper.Similarly,inhisVolumeIIof1904,PfefferusedthetermphotosynthesisafewtimeswithoutcitingBarnes,andcontinuedtousetheword‘assimilation.’Inhis1898paper,Barnesfeltobligedtosay:‘ImayheretakeoccasiontocriticizePfeffer’sdefenceofthetermassimilation.’Thisstatementisfollowedbycarefullyreasonedargumentsforabandoning‘assimilation’todescribetheplantprocess.Weoweadebtofgrati-tudetoCharlesBarnes,whowascourageousenoughtocriticizeoneofthe‘giants’ofplantphysiologyinhistime.EvolutionofthedeÞnitionofphotosynthesisThedenitionofphotosynthesisproposedbyBarnesin1893isgiven,essentiallyunchanged,innumerousdictionariesuptothepresenttime(seeGest2001).TheOxfordEnglishDictionary(OED)isconsideredtobethemostauthoritativedictionaryoftheEng-lishlanguageanditssecondedition(1989)denesbiologicalphotosynthesisasfollows:‘Theprocessbywhichcarbondioxideisconvertedintoorganicmatterinthepresenceofthechlorophyllofplantsundertheinuenceoflight,whichinallplantsex-ceptsomebacteriainvolvestheproductionofoxygenfromwater.’Thisclumsydenitioncontainsthecuri-ousphrase‘inallplantsexceptsomebacteria,’whichincorrectlyimpliesthatbacteriaareplants.TheOEDisalsoincorrectincitingBarnes1898astherstuseof‘photosynthesis’;thecorrectreferenceisBarnes1893.Thediscoveryofanoxygenicbacterialphotosyn-thesismadethegeneraldenitionof‘photosynthesis’intheOEDandmostotherdictionariesincorrect,butthisisstillnotwidelyrecognized.Tenyearsbe-foreBarnes(1893)coinedtheterm‘photosynthesis,’TheodorEngelmann(1883)reportednovelexperi-mentsthatrevealedphotosensorybehaviorofpurplesulfurbacteria(seedescriptioninGest1995).Theseexperimentssuggestedthatthebacteriawerephoto-syntheticorganisms,butdoubtswereraisedbecauseEngelmann’stestsforOproductiongavenegativeresults.Later,in1907,H.Molischdemonstratedcon-vincinglythatpurplebacteriadonotproduceOandthattheyhavethecapacitytouseorganiccom-poundsassolecarbonsourcesforgrowthwithen-ergyprovidedbylight(Molisch1907).Thus,themetabolic/physiologicalpatternofthepurplebacteriaobviouslydidnotsatisfythecriteriaforphotosyn-thesisasoriginallydenedforgreenplants,andasaconsequence,forseveraldecadesthebacteriawerenotgenerallyacceptedasbeingphotosynthetic.Theoriginaldenitionofphotosynthesisasanoxygenicprocessledinvestigatorstocontinuedesigningfu- tileexperimentstondevidenceofOproductionbypurplebacteriaforsometime.Thelastdenitivenegativeexperimentswerereportedin1954,71yearsafterEngelmann’srstreport!(seediscussioninGestThediscoveryofphotophosphorylationin1954re-vealedabasic‘commondenominator’ofoxygenicandanoxygenicphotosyntheses,andpavedthewayforredenitionof‘photosynthesis.’In1963,MartinKa-mensuggestedareviseddenitionwhichwouldhavetheeffectofincludinganoxygenicbacterialphotosyn-thesisby(a)avoidinganyspecicationofthecarbonsourceforgrowth,and(b)notindicatingOasapho-tosyntheticproduct.Kamen’sdenitionis:‘Photosyn-thesisisaseriesofprocessesinwhichelectromagneticenergyisconvertedtochemicalfreeenergywhichcanbeusedforbiosynthesis.’Kamenrecognizedthathehadoffereda‘rathernoncommittaldenition,’andinfactitdoesnotconveytheessentialcharacteroftheanoxygenicphototrophiclifemode.Thirtyyearslater,IconcludedthatKamen’sden-itionrequiredfurthersharpening,andsuggestedthefollowinggeneraldenition(Gest1993):Photosynthesisisaseriesofprocessesinwhichelectromagneticenergyisconvertedtochemicalenergyusedforbiosynthesisoforganiccellma-terials;aphotosyntheticorganismisoneinwhichamajorfractionoftheenergyrequiredforcellularsynthesesissuppliedbylight.MolecularoxygenandCOarenotincludedinthe‘commondenominatordenition’ofphotosynthesisbecausephotosyntheticbacteriadonotproduceOandCOisnotnecessarilyarequiredcarbonsource.Anumberofthebacterialspeciescangrowwitheithersimpleorganiccompounds,suchasacetate,asthesolecarbonsourceforsynthesisofallcellconstituentsusinglightasthesourceofenergy.Includingthedenitionofaphotosyntheticorgan-isimportantbecauseoftherecentdiscoveryofanumberofaerobicbacterialspecieswhichcontainbacteriochlorophyllandcarotenoids,butwhichareincapableofusinglightasthesoleormajorsourceofenergyforgrowth.Ihavedescribedsuchorgan-ismsas‘quasi-photosyntheticbacteria’(Gest1993).J.ThomasBeattysuggestsdesignatingthemas‘aer-obicphototrophicbacteria’(seeJ.T.Beatty,thisissue).‘Phototrophic’inthiscontextistakentomeanthatsuchorganismsundercertainconditionscanuselightasasupplementalenergysupply,butnotnecessarilyasamajorsource.TheimportanceofdeÞnitionsAntoineLavoisier,whorevolutionizedthescienceofchemistryinthe18thcenturyandreplacedthemythical‘phlogiston’withtheterm(andconcept)ofoxygen,clearlyunderstoodtheimportanceofaccuratedenitions.Inhiswords:‘Wecannotimprovethelan-guageofanysciencewithoutatthesametimeimprov-ingthescienceitself;norcanwe,ontheotherhand,improveasciencewithoutimprovingthelanguageornomenclature’(Lavoisier1790).AcknowledgmentsIamindebtedtoRogerBeckman,Head,LifeSci-encesLibrary,IndianaUniversity,Bloomington,forskilfulelectronicsearchesoftheliterature.ResearchoftheauthoronphotosyntheticbacteriaissupportedbyNationalInstitutesofHealthGrantGM58050.ThismanuscriptwaseditedbyGovindjee.ReferencesAnonymous(1910)CharlesReidBarnes.BotGaz49:321–324BarnesCR(1893)Onthefoodofgreenplants.BotGaz18:403–411BarnesCR(1896)Photosyntaxphotosynthesis.BotanicalpapersatBuffalo.BotGaz22:248BarnesCR(1898)So-called‘Assimilation’.BotanCentralblatt76:BlackmanFFandMatthaeiGLC(1905)Experimentalresearchesinvegetableassimilationandrespiration.IV.Aquantitativestudyofcarbon-dioxideassimilationandleaf-temperatureinnaturalillumination.ProcRSocLondonSerB76:402–460EngelmannTW(1883)Bacteriumphotometricum.EinBeitragzurvergleichendenPhysiologiedesLicht-undFarbensinnes.ArchPhysiol30:95–124EwartAJ(1900)ThePhysiologyofPlants.ATreatiseupontheMetabolismandSourcesofEnergyinPlants.[Englishtranslationofthe‘Handbuch’byW.Pfeffer].ClarendonPress,OxfordGestH(1988)Sun-beams,cucumbers,andpurplebacteria.Photo-synthRes19:287–308GestH(1993)Photosyntheticandquasi-photosyntheticbacteria.FEMSMicrobiolLett112:1–6GestH(1995)Phototaxisandothersensoryphenomenainpurplephotosyntheticbacteria.FEMSMicrobiolRev16:287–294GestH(2001)Evolutionofknowledgeencapsulatedinscienticdenitions.PerspBiolMed44:556–564HansenXX(1898)ReviewofPfeffer’sPanzenphysiologie(revisededition,1897).BotanischeZeitung56:II(2:22–24)[Note:thepaperdoesnothavetheinitialsoftheauthor;thus,XXhasbeenaddedtoindicatethatfact.]KamenMD(1963)PrimaryProcessesinPhotosynthesis.AcademicPress,NewYorkLavoisierA(1790)ElementsofChemistry,trans.byR.Kerr.Creech,EdinburghMolischH(1907)DiePurpurbakteriennachneuenUntersuchungen.GustavFischer,JenaOxfordEnglishDictionary(1989)2nded.ClarendonPress,Oxford