the pyrenoid is a carbon-fixing liquid dropletsep 21, 2017 · plants and algae use the enzyme...
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PressRelease,September21,2017
Thepyrenoidisacarbon-fixingliquiddroplet
PlantsandalgaeusetheenzymeRubiscotofixcarbondioxide,removingitfromtheatmosphereand converting it into biomass. However, Rubisco performs this reaction slowly and can alsohave unwanted reactions with oxygen. Algae have figured out a clever way to prevent theoxygenreactionandincreasetheefficiencyofcarbonfixation.TheygathermostoftheirRubiscointo a ball-shapedmicrocompartment called thepyrenoid,which they floodwith a high localconcentrationofcarbondioxide. Ifwelearnhowalgaebuildthepyrenoid,wemaybeabletoengineer it intoplants, creatingcrops that removemorecarbondioxide fromtheatmospherewhile producing more food. Combining genetics, cell biology, computer modeling and cryo-electron tomography,an international teamof scientistsatPrincetonUniversity, theCarnegieInstitution for Science, Stanford University and theMax Plank Institute of Biochemistry haveunravelled the mysteries of how the pyrenoid is assembled. They found that the pyrenoidbehaveslikeadropletofliquid,whichdissolvesduringcelldivisiontoensurethatitisinheritedbybothdaughtercells.ThisstudyispublishedinthejournalCell.AwarmingplanetOurplanet’sclimate ischanging.Eachyearbrings recordhigh temperatures thatcauseextremeweather,meltingpolar ice and risingocean levels.Globalwarming is intensifiedby greenhousegasses such as carbon dioxide, which prevent the escape of heat from our atmosphere. Usingenergyfromthesuninaprocesscalledphotosynthesis,plantsandalgaeactasnaturalairfilters,removingcarbondioxidefromtheatmospherewhilereplacingitwiththeoxygenthatwebreathe.AbouthalfofthephotosynthesisonEarthisperformedintheoceanbysingle-celledalgae.ManyofthesealgaefixcarbondioxidemoreefficientlythanlandplantsbyconcentratingmostoftheirRubisco intoamicrocompartment calledapyrenoid.Despite the importanceof thepyrenoid totheglobalenvironment,untilrecently,itwasunknownhowthismicrocompartmentassembles.VisualizingeveryRubiscowithinthepyrenoidThe first breakthrough in understanding pyrenoid assembly came when the team of MartinJonikas, leaderof theCarnegie/StanfordandPrincetongroups, identifieda linkerprotein in thegreen algaChlamydomonas that binds Rubisco enzymes togetherwithin the pyrenoid.Without
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this“molecularglue,”thepyrenoiddoesnotform.However, itwasnotknownhowtheRubiscoproteinsareorganizedwithinthepyrenoid,withclassicalelectronmicroscopystudiessuggestingthatthepyrenoidisahighlyorderedsolidcrystal.To answer this question, the team lead by Benjamin Engel at the Max Planck Institute ofBiochemistry used cryo-electron tomography to examine the molecular organization of thepyrenoidwithinChlamydomonascellsthatwerefrozenintheirnativestate,avoidingtheartefactscaused by sample preparation for classical electron microscopy. This high-resolution imagingtechniqueenabledEngel and colleagues topreciselymeasure thepositionsof the thousandsofRubisco enzymes within the pyrenoid. Instead of crystalline organization, they found that thepyrenoidonlyhasshort-rangeorder.Engelexplainsthisresult:"Ifyoucompareourmeasurementstotheorganizationofmoleculesinsideliquids,thereareveryclearsimilarities.Thissuggeststhatpyrenoidsareactuallyliquid-likestructures."LikeoilandwaterIn order to prove that the pyrenoid behaves like a liquid, Elizabeth Freeman Rosenzweig, firstauthor of the study, used fluorescencemicroscopy tomeasureRubiscomovementwithin livingcells. She used a high-powered laser to destroy the signal from fluorescent labels attached toRubisco inhalfof thepyrenoid,while leaving thesignal in theotherhalfof thepyrenoid intact.Within minutes, the fluorescence spread throughout the pyrenoid, showing that the enzymesmovearoundastheywouldinaliquid.Thus,thepyrenoidisaliquidmicrocompartmentfloatingwithin a second larger liquid compartment, the chloroplast. This is an example of “phaseseparation,” a physical phenomenon that has recently been shown to play a role incompartmentalizingmanyofthecell’sproteins.FreemanRosenzweigusesananalogytoexplainhowitworks:“Althoughtheforcesthatcausethepyrenoid’sphaseseparationaredifferent,itiseasytothinkaboutittermsofafamiliarimage:adishofoilandvinegarthatyoumightgetatanItalian restaurant. The oil and vinegar are both liquids, but they don’tmix. The vinegar insteadformsdropletsthatfloatinthepoolofoil.Similarly,wethinkthepyrenoidformsadropletwithintheliquidenvironmentofthechloroplast.”FreemanRosenzweigalsodiscoveredthatthereisaspecialtimewhenthe“oil”ofthechloroplaststroma and the “vinegar” of the pyrenoid do mix. As the single-celled algae divide into twodaughter cells, the pyrenoid undergoes a “phase transition,” partially dissolving into thesurrounding stroma of the chloroplast. Ordinarily, the remaining pyrenoid is pinched into two,witheachdaughtercellreceivinghalf.However,sometimesthisdivisionfails, leavingoneofthedaughtercellswithnopyrenoid.Theresearchersobservedthatcellsthatfailedtoreceivehalfofthepyrenoidcouldstillformonespontaneously,ordenovo.Theysuspectthateachdaughtercellreceivessomeofthedissolvedpyrenoidcomponents,andthatthesecomponentscancondenseintoanewpyrenoidthewaythatraindropscondensefromwatervapor.“Wethinkthepyrenoiddissolutionbeforecelldivisionandcondensationafterdivisionmaybearedundantmechanismto
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ensurethatbothdaughtercellsgetpyrenoids,” Jonikassaid.“Thatway,bothcellswillhavethiskeyorganellethat'scriticalforassimilatingcarbon.”BettercropsforachangingworldJonikasandhisteamhavebigplansfortheapplicationsofthisknowledge.Theywanttoengineerpyrenoids into crops such aswheat and rice to address problems including climate change andworldhunger.“Understandinghowalgaecanconcentratecarbondioxideisakeysteptowardthegoalofimprovingphotosynthesisinotherplants,”Jonikassaid.“Ifwecouldengineerothercropstoconcentratecarbon,wecouldaddressthegrowingworlddemandforfood.”TheJonikasgrouphasevencreatedtheirownmascot,SammytheChlamy,whousesamusicvideototeachusaboutthepowerofthepyrenoid:https://www.youtube.com/watch?v=B2ftWvnBanYSome portions of this article were provided courtesy of the Princeton University Office ofCommunications.ThemusicvideowascreatedbyJonathanMann.[SiM]---AboutBenjaminEngelBenjamin Engel’s work focuses on characterizing the molecular architecture of organelles,includingthechloroplast.Usingcryo-electrontomography,heandhis teamareable tovisualizemacromolecular complexes within the native cellular environment with high spatial resolution.Engel completed his undergraduate studies in Molecular and Cell Biology at the University ofCalifornia, Berkeley, in theUnited States. In 2011, he received his Ph.D. from theUniversity ofCalifornia, San Francisco. Since then, he hasworked as a postdoctoral fellow in the “MolecularStructural Biology” department of Wolfgang Baumeister at the Max Planck Institute forBiochemistry inMartinsriednearMunich.HewasawardedtheHumboldtPostdoctoralResearchFellowshipandMPIBJuniorResearchAward.AbouttheMaxPlanckInstituteofBiochemistryThe Max Planck Institute of Biochemistry (MPIB) belongs to the Max Planck Society, anindependent,non-profitresearchorganizationdedicatedtotoplevelbasicresearch.AsoneofthelargestInstitutesoftheMaxPlanckSociety,850employeesfrom45nationsworkhereinthefieldof life sciences. In currently eight departments and about 25 research groups, the scientistscontribute to the newest findings in the areas of biochemistry, cell biology, structural biology,biophysicsandmolecularscience.TheMPIBinMunich-Martinsriedispartofthelocallife-science-campus where two Max Planck Institutes, a Helmholtz Center, the Gene-Center, several bio-medical facultiesof twoMunichuniversitiesand severalbiotech-companiesare located in closeproximity.(http://biochem.mpg.de)
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AboutMartinJonikasMartinJonikasisanAssistantProfessoratPrincetonUniversity.Hislaboratoryaimstotransformourunderstandingof photosynthetic eukaryotesbydeveloping and applying cutting-edge tools.He studied aerospace engineering as an undergraduate at the Massachusetts Institute ofTechnology.He then receivedhis Ph.D. in 2009 from theUniversity of California, San FranciscoworkingwithJonathanWeissman,MayaSchuldinerandPeterWalteronhigh-throughputgeneticsand protein folding in the endoplasmic reticulum. Jonikas did not do a postdoc and started hislaboratorydirectlyafterobtaininghisPh.D., asa facultymemberat theCarnegie Institution forScience and an Assistant Professor by courtesy at Stanford University. After seven years atCarnegie,hemovedhislaboratorytoPrinceton.Heistherecipientofseveralawards,includinga2016 Howard Hughes Medical Institute-Simons Foundation Faculty Scholar Award, a 2015 NIHNewInnovatorAwardanda2010AirForceYoungInvestigatorAward.
CaptionThisimagedepictsarenderingofacryo-electrontomogramofaChlamydomonaspyrenoid,withtubulemembranes(greenandyellow)awashina“sea”ofRubiscoenzymes(blue).BenjaminEngelandcolleaguesfoundthatRubiscoproteinsinthepyrenoidarepackedtogetherlikealiquid.©ScienceDirect
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CaptionInthisimage,SammytheChlamyillustrateshowthepyrenoidisaphase-separatedmicrocompartmentwithinthechloroplastoftheChlamydomonascell.©KrystalKlausOriginalpublication:E.S.FreemanRosenzweig,B.Xu,L.KuhnCuellar,A.Martinez-Sanchez,M.Schaffer,M.Strauss,H.N.Cartwright,P.Ronceray,J.M.Plitzko,F.Förster,N.S.Wingreen,B.D.Engel,L.C.M.Mackinder&M.C.Jonikas.“TheEukaryoticCO2-ConcentratingOrganelleisLiquid-LikeandExhibitsDynamicReorganization”.Cell,September2017DOI:10.1016/j.cell.2017.08.008 Contact:Dr.BenjaminEngel Dr.ChristianeMenzfeldDept.ofMolecularStructuralBiology PublicRelationsMaxPlanckInstituteofBiochemistry MaxPlanckInstituteofBiochemistryAmKlopferspitz18 AmKlopferspitz1882152Martinsried 82152MartinsriedGermany GermanyTel.+49898578-2653 Tel.+49898578-2824E-Mail:[email protected] E-Mail:[email protected] www.biochem.mpg.de