Respiration in Archaea and Bacteria
Advances in Photosynthesis and Respiration VOLUME 16 Series Editor: GOVINDJEE University of Illinois, Urbana, Illinois, U.S.A.
Consulting Editors: Christine FOYER, Harpenden, U.K. Elisabeth GANTT, College Park, Maryland, U.S.A. John H. GOLBECK, University Park, Pennsylvania, U.S.A. Susan S. GOLDEN, College Station, Texas, U.S.A. Wolfgang JUNGE, Osnabrück, Germany Hartmut MICHEL, Frankfurt am Main, Germany Kirmiyuki SATOH, Okayama, Japan James Siedow, Durham, North Carolina, U.S.A.
The scope of our series, beginning with volume 11, reflects the concept that photosynthesis and respiration are intertwined with respect to both the protein complexes involved and to the entire bioenergetic machinery of all life. Advances in Photosynthesis and Respiration is a book series that provides a comprehensive and state-of-the-art account of research in photosynthesis and respiration. Photosynthesis is the process by which higher plants, algae, and certain species of bacteria transform and store solar energy in the form of energy-rich organic molecules. These compounds are in turn used as the energy source for all growth and reproduction in these and almost all other organisms. As such, virtually all life on the planet ultimately depends on photosynthetic energy conversion. Respiration, which occurs in mitochondrial and bacterial membranes, utilizes energy present in organic molecules to fuel a wide range of metabolic reactions critical for cell growth and development. In addition, many photosynthetic organisms engage in energetically wasteful photorespiration that begins in the chloroplast with an oxygenation reaction catalyzed by the same enzyme responsible for capturing carbon dioxide in photosynthesis. This series of books spans topics from physics to agronomy and medicine, from femtosecond processes to season long production, from the photophysics of reaction centers, through the electrochemistry of intermediate electron transfer, to the physiology of whole orgamisms, and from X-ray christallography of proteins to the morphology or organelles and intact organisms. The goal of the series is to offer beginning researchers, advanced undergraduate students, graduate students, and even research specialists, a comprehensive, up-to-date picture of the remarkable advances across the full scope of research on photosynthesis, respiration and related processes. The titles published in this series are listed at the end of this volume and those of forthcoming volumes on the back cover.
Respiration in Archaea and Bacteria Diversity of Prokaryotic Respiratory Systems
Edited by
Davide Zannoni Universita di Bologna, Italy
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 1-4020-2002-3 (HB) ISBN 1-4020-3163-7 (e-book) Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands. Sold and distributed in North, Central and South America by Springer, 101 Philip Drive, Norwell, MA 02061, U.S.A. In all other countries, sold and distributed by Springer, P.O. Box 322, 3300 AH Dordrecht, The Netherlands.
The camera ready text was prepared by Lawrence A. Orr, Center for the Study of Early Events in Photosynthesis, Arizona State University, Tempe, Arizona 85287-1604, U.S.A.
Printed on acid-free paper
All Rights Reserved © 2004 Springer No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Printed in the Netherlands.
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STRAIN*7 STRONGLYSUGGESTINGTHEPRESENCEOFA BC LIKECOMPLEXADDITIONALSUPPORTCOMESFROMTHE REPORTEDSENSITIVITYTOANTIMYCIN&ROMNONEOFTHE ARCHAEALORGANISMSAFUNCTIONALCOMPLEXCOULDBE ISOLATEDSOFAR(OWEVER AFUNCTIONALEQUIVALENTTOA RESPIRATORYCOMPLEX)))ISOBVIOUSLYINCLUDEDINTHE SUPERCOMPLEX3OX-ASTOBEDISCUSSEDINASUBSE QUENTPARAGRAPH)NTHEFOLLOWING SINGLECONSTITUENTS OFPOSSIBLEARCHAEALEQUIVALENTSTOCOMPLEX)))ARE DISCUSSEDASWELLASTHEIRFUNCTIONALSIGNIlCANCE " "SDIBFBM3JFTLF1SPUFJOT 4HE UNIQUE ELECTRONIC STRUCTURE OF THE TYPICAL &E3 CLUSTERINRESPIRATORY2IESKEPROTEINSISGENERATEDBY THEMIXEDLIGANDATIONOFTWO&EIONSBYTWOHISTIDINES ONONESIDE ANDTWOCYSTEINESONTHEOTHER WITHTWO SULFURIONSBRIDGINGTHE&EIONS4HISCOORDINATION GIVES RISE TO A CHARACTERISTIC %02 SPECTRUM WHICH ISSTRONGLYDIFFERENTFROMTHOSEOFOTHERIRON SULFUR CLUSTERS 4HE HIGHLY RESOLVED 8 RAY STRUCTURE OF MITOCHONDRIAL BC COMPLEXES COULD BE DETERMINED 8IAETAL "ERRYETAL (UNTE REVEALINGTWOOREVENTHREE-ONTOYAETAL QUINOLQUINONE BINDING SITES AND THE SURPRISING FACT THAT THE PRIMARY ELECTRON ACCEPTOR FOR QUINOL
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OXIDATION THE2IESKEPROTEIN ACTSASAREORIENTING REDOXDOMAINBETWEENTHESITEOFELECTRONINPUTAND THE ACCEPTOR CYTOCHROME C 3NYDER ET AL 4HESECONDELECTRONOFAQUINOLISTRANSFERREDTOTHE B TYPECYTOCHROMEFORFURTHERMECHANISTICDETAILS SEE8IAETAL 9UETAL $ARROUZETETAL 'UTIERREZ #IRLOS AND4RUMPOWER SEE ALSO#HAPTERBY#OOLEYETAL 6OL 4HElRSTARCHAEALRESPIRATORY2IESKEPROTEINWAS PURIlEDFROM3ACIDOCALDARIUS3CHMIDTETAL 3URPRISINGLY ASECOND2IESKEPROTEINWASDETECTED INTHESAMEORGANISMASACONSTITUENTOFTHE3OXRESPIRATORYCOMPLEX#ASTRESANAETAL 3CHMIDT ET AL 4HESE THE 3OX, AND 3OX& 2IESKE
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TIONATYPICALPARTIALALIGNMENTISSHOWNIN&IG !COMPREHENSIVEREVIEWONSEQUENCEFEATURESAND THEPHYLOGENETICRELATIONOF2IESKEPROTEINS 2IESKE TYPE PROTEINSAND2IESKE LIKEFERREDOXINSISGIVENIN 3CHMIDTAND3HAW 4HE ONLY $ STRUCTURE WITH ATOMIC RESOLUTION OF AN !RCHAEAL 2IESKE PROTEIN HAS RECENTLY BEEN DETERMINED FOR 3OX& FROM 3 ACIDOCALDARIUS THE . TERMINAL MEMBRANE ANCHOR HAS BEEN TRUNCATED "ÚNISCHETAL "ÚNISCHETAL 4HIS¯ STRUCTURE GIVES A HINT ON THE STRUCTURAL DIFFERENCES IMPOSED BY THE LARGE SEQUENCE INSERTION SEE &IG ASDEMONSTRATEDIN&IG!NADDITIONAL ` SHEET `# ISINSERTEDBETWEENNORMALLYPRESENT `AND `ASWELLASANADDITIONALDISULlDEBRIDGEBETWEEN #YSAND#YS4HISENABLESAlRMlXATIONOF THE# TERMINUSTOGETHERWITHTHE( BONDINTERACTION BETWEEN ` `ANDMAYCONTRIBUTETOTHEENORMOUS HEAT STABILITY )MPORTANTLY THE . TERMINUS AND THE ADJACENT HINGE REGION NECESSARY FOR A LARGE SCALE DOMAINMOVEMENT)WATAETAL ARENOTlXED INTHESAMEWAY&URTHER A HELIXNOTFOUNDIN OTHERKNOWN2IESKEPROTEINS)WATAETAL 8IA ETAL (UNTE ISPRESENTINTHIS!RCHAEAL PROTEIN&ORADETAILEDSTRUCTURALALIGNMENTTHEREADER ISREFERREDTO$ARROUZETETAL )NCOMPARISON TOTHE!RCHAEAL2IESKEPROTEINTHOSEFROMSPINACH B FORBOVINE F BCCOMPLEXESDISPLAYAMUCHLOWER PACKINGDENSITYOFTHEIR$STRUCTURE #"TTPDJBUFEC$ZUPDISPNFTBOEB/PWFM $PNQMFY &OR A DECISIVE ANSWER TO THE ABOVE QUESTION THE ARCHAEAL2IESKEPROTEINSHAVETOBESEENINAMORE GENERAL CONTEXT ALONG WITH THEIR PROTEIN CHEMICAL ANDGENETICENVIRONMENT!GAIN THEBESTINVESTIGATED EXAMPLEISTHETHERMOACIDOPHILICARCHAEON3ULFOLOBUS ACIDOCALDARIUS WHEREGENETIC TRANSCRIPTIONAL PRO TEINCHEMICAL ANDFUNCTIONALSTUDIESARESUPPORTING EACHOTHER %ARLIER A MONO HEME B TYPE CYTOCHROME FROM 3 ACIDOCALDARIUS ;#YT B= HAS BEEN DESCRIBED TOGETHER WITH ITS GENES CBS! AND CBS" (ETTMANN ETAL :ÊHRINGERETAL 4HEFUNCTIONOF THISHIGHLYGLYCOSYLATEDPROTEINWASNOTKNOWN4HIS CYTOCHROME IS AN INTEGRAL MEMBRANE PROTEIN WITH ITSHEMEBEARINGDOMAINFACINGTHEOUTERSURFACEOF THEPLASMAMEMBRANEITISABUNDANTIN3ULFOLOBUS MEMBRANES GROWING UNDER LIMITED OXYGEN SUPPLY 4HEDISCOVERYTHATITISPARTOFAGENECLUSTERALSO
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n
3ACIDOCALDARIUS
3OX, RECOMB
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INMEMBRANE
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n
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n
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0AEROPHILUM
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0AEROPHILUM
0A2RECOMB 6n&7
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n
n
n
(SALINARUM
INMEMBRANE
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n
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n
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3TOKODAII
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n
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ND
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HEME ./COMPLEXESSUGGESTSTHATFORMATIONOFSUCH ASPECIESDURINGCATALYSISWOULDLEADTOANINHIBITED ENZYMEFROMWHICH./RELEASEWOULDBEVERYSLOW 4HUS WE MIGHT EXPECT CYTOCHROME CD TO HAVE AN IMPORTANTDESIGNFEATUREFORAVOIDINGTHEFORMATION OFFERROUSD HEME ./COMPLEX4HESLOWRATEOF INTER HEME ELECTRON TRANSFER HAS SUGGESTED SUCH A MECHANISM"UTTHEOFTENOBSERVEDFORMATIONOFTHE FERROUS D HEME ./COMPLEXSUGGESTTHATEXPERIMEN TALCONDITIONSWHICHWOULDPROMOTETHERELEASEOF ./HAVENOTYETBEENIDENTIlED!ROLEFORTYROSINE INDISPLACINGNITRICOXIDENOWSEEMSLESSLIKELY ASTHE9VARIANTENZYMEISFULLYACTIVE'ORDON ETAL )NORIGINALSTOPPED mOWRAPIDREACTIONSTUDIESON CYTOCHROME CD FROM 0 AERUGINOSA THE FERROUS D HEME ./SPECIESWASFORMEDDESPITETHEELECTRON TRANSFERFROMTHEC TOTHE D HEMEBEINGRELATIVELY SLOW RATECONSTANTAPPROXIMATELYSn GIVENTHERELA TIVELYSHORTDISTANCEBETWEENTHETWOHEMES3UCHA DISTANCEWOULDNORMALLYPREDICTMUCHFASTERELECTRON TRANSFERRATES4HISRELATIVELYSLOWINTER HEMEELECTRON TRANSFERRATEHASBEENFREQUENTLYOBSERVEDANDBEFORE THESTRUCTUREOFTHEPROTEINWASKNOWNWASTHOUGHTTO REmECTRELATIVELYLARGEINTER HEMESEPARATIONDISTANCE ANDORRELATIVEORIENTATIONOFTHETWOHEMESTHATWAS NOTCONDUCIVETORAPIDELECTRONTRANSFER-AKINENET AL 4HECRYSTALSTRUCTURESPROVIDENOEVIDENCE FOREITHEROFTHESEPROPOSALSTHEREISNOTHINGUNUSUAL ABOUTTHERELATIVEORIENTATIONOFTHE CANDDHEME GROUPS!SLOWELECTRONTRANSFERRATEMUST THEREFORE BEREGARDEDASDIAGNOSTICOFRATE LIMITINGCHEMICAL STEPSATTHED HEMECENTER &URTHERRAPIDREACTIONANALYSISOFTHE 0AERUGINOSA ENZYME HAS RECENTLY BEEN REPORTED #UTRUZZOLA ET AL -IXINGOFTHEFULLYREDUCEDENZYMEWITH BETWEENAND+-NITRITEWASFOLLOWED JUDGED BYVISIBLEABSORPTIONSPECTRA BYNITRITEBINDINGTOTHE ACTIVESITEONTHEMSECTIMESCALE4HISWASFOLLOWED ONTHETOSECTIMESCALEBYOXIDATIONOFTHE C HEMETOGIVEENZYMETHATHADNITRICOXIDEBOUND TOTHEDHEME4HISISRATHERSLOWIFTHEENZYMEIN STEADYSTATEISTOTURNOVERMANYTIMESPERSECOND 3UBSEQUENTLY ATTIMESBETWEENSANDMINTHE ENZYMEWASFULLYREDUCEDBYTHEASCORBATEPRESENTTO GIVEESSENTIALLYADEADENDCOMPLEXWITH NITRICOXIDE BOUNDTOTHEFERROUSHEME4HECHANGESINTHERATES OFTHESESTEPSWEREALSOREPORTEDFORMUTANTFORMS OFTHEENZYMETHATEACHLACKEDONEOFTHETWOACTIVE SITEHISTIDINELIGANDS 4HE lRST RAPID REACTION STUDY OF THE REDUCTION
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)NSUMMARY THEREISSTILLMUCHTOUNDERSTANDABOUT THE NITRITEREDUCTIONREACTION4HECRYSTALSTRUCTURES HAVESHOWNHOWNITRITECANBINDTOTHED HEMEIRON ANDPROTONSCANBEPROVIDEDTOONEOFITSOXYGENATOMS FROMTWOHISTIDINERESIDUES(OWEVER ASYETNORAPID REACTION STUDY HAS DETECTED THE RELEASE OF PRODUCT NITRICOXIDERATHERTHATTHEFORMATIONOFTHEINHIBITORY DEAD ENDFERROUSD HEME ./COMPLEX)TISALSONOT CLEARWHYTHERATEOFINTER HEMEELECTRONTRANSFERIS SOSLOWOVER¯WHENNITRITEORNITRICOXIDEISTHE LIGANDTOTHE D HEME5NDERSTANDINGTHESEISSUESAND ALSOTHEROLEOFTHEmEXIBILITYOFTHECHEMEDOMAIN REMAINMAJORCHALLENGESFORTHEFUTURE &MFDUSPO%POPSTUP$ZUPDISPNFDE/JUSJUF 3FEVDUBTF !SMENTIONEDINTHE)NTRODUCTION NITRITEREDUCTASESFOR WHICHNITRICOXIDEISTHEREACTIONPRODUCTARELINKED TO THE UNDERLYING RESPIRATORY CHAIN AT THE LEVEL OF C TYPE CYTOCHROMES ANDOR CUPREDOXINS 4HUS THE ELECTRONS DESTINED FOR CYTOCHROME CD PASS THROUGH THECYTOCHROMEBC COMPLEX(OWTHEYPASSONFROM THIS COMPLEX TO CYTOCHROME CD IS STILL A MATTER OF
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$IBQUFS $ZBOPCBDUFSJBM3FTQJSBUJPO 4HEGENESENCODING#OXCONSTITUTEANOPERON AS HASBEENDEMONSTRATEDFORTHECOX"!#GENESOF # 3YN ECHOCYSTISSP0##(OWITTAND6ERMAAS # 3CHMETTERERETAL ANDCOX"!# THE COX"!# 0ILSANDCOLLABORATORS UNPUBLISHED GENESOF!NA BAENAVARIABILIS!4##ANDTHE COX"!# # GENES OF!NABAENA SP0##6ALLADARESETAL (OWEVER THEPRIMARYTRANSCRIPTCOULDBEPROCESSED IN !NABAENASTRAINS SINCEASTRONGSIGNALIN.ORTHERN BLOTSWASOBTAINEDFORANM2.!CONTAININGONLYTHE lRSTGENEOFTHEOPERON THE COX" GENE7HETHERTHIS ISOFFUNCTIONALSIGNIlCANCEINTHECELLSCANNOTBE STATEDCURRENTLY ESPECIALLYASITISEXPECTEDTHATTHE THREESUBUNITSARESYNTHESIZEDINEQUALAMOUNTSIN VIVO#YTOCHROMECOXIDASEISSUBJECTTOGENEREGULA TIONINRESPONSETOTHEGROWTHMEDIUMIN !NABAENA STRAINS )N ! VARIABILIS !4## THE COX"!# GENES ARE UPREGULATED BY FRUCTOSE 3CHMETTERER ET AL BUTTHISREGULATIONOCCURSONLYWITHONE OFTHETWOTRANSCRIPTIONALSTARTSITESUPSTREAMOFCOX" TSP WHILETHEOTHERONETSP ISCONSTITUTIVE)N # GENES AND !NABAENA SP 0## THE COX"!# ALSO THE COX"!# # GENES ENCODING THE !24/ SEE BELOW AREUPREGULATEDWHENTHECELLSAREGROWNIN THEABSENCEOFCOMBINEDNITROGENANDTHUSCONTAIN HETEROCYSTS6ALLADARESETAL 4HE COX"!# GENESAREEITHERPREFERENTIALLYORPOSSIBLYEVENEX CLUSIVELYEXPRESSEDIN HETEROCYSTS -UTANTS LACKING CYTOCHROME C OXIDASES HAVE BEENCONSTRUCTEDINSTRAINS 3YNECHOCYSTIS SP0## 3CHMETTERER ET AL 0ILS ET AL !NABAENASP0##6ALLADARESETAL !NABAENA VARIABILIS!4## 3CHMETTERER ET AL 0ILSANDCOLLABORATORS UNPUBLISHED AND 3YNECHOCOCCUS SP0##.OMURA 4HESE MUTANTSHAVEALLOWEDTODETERMINETHAT CYTOCHROME C OXIDASEISTHEMOSTIMPORTANTRESPIRATORYTERMINAL OXIDASEWITHRESPECTTOBIOENERGETICCAPACITY7HEN THEGENESENCODINGCYTOCHROME C OXIDASEWEREIN ACTIVATEDIN 3YNECHOCYSTISSP0##COX"!# # ORIN!NABAENAVARIABILIS COX"!# THERESULTING # MUTANTSLOSTTHECAPACITYFORHETEROTROPHICGROWTH 4HISISESPECIALLYSTRIKINGFORTHELATTERSTRAIN SINCE ITCONTAINSATLEASTONEOTHERCYTOCHROME C OXIDASE COX"!# )N # 3YNECHOCYSTIS SP0## THELOSS OF#OXALSOLEDTOTHELOSSOFTHESO CALLEDSALTRES PIRATION A SHORT TERM ENHANCEMENT OF RESPIRATORY ACTIVITYUPONTHEADDITIONOF.A#L EVENIFTHEOTHER TWORESPIRATORYTERMINALOXIDASESWERESTILLPRESENT)N !NABAENASP0##THECOXLOCUSISINVOLVEDIN THEPROTECTIONOFNITROGENASEIN HETEROCYSTSFROMTHE
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Advances in Photosynthesis Series editor: Govindjee, University of Illinois, Urbana, Illinois, U.S.A. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
D.A. Bryant (ed.): The Molecular Biology of Cyanobacteria. 1994 ISBN Hb: 0-7923-3222-9; Pb: 0-7923-3273-3 R.E. Blankenship, M.T. Madigan and C.E. Bauer (eds.): Anoxygenic Photosynthetic Bacteria. 1995 ISBN Hb: 0-7923-3681-X; Pb: 0-7923-3682-8 J. Amesz and A.J. Hoff (eds.): Biophysical Techniques in Photosynthesis. 1996 ISBN 0-7923-3642-9 D.R. Ort and C.F. Yocum (eds.): Oxygenic Photosynthesis: The Light Reactions. 1996 ISBN Hb: 0-7923-3683-6; Pb: 0-7923-3684-4 N.R. Baker (ed.): Photosynthesis and the Environment. 1996 ISBN 0-7923-4316-6 P.-A. Siegenthaler and N. Murata (eds.): Lipids in Photosynthesis: Structure, Function and Genetics. 1998 ISBN 0-7923-5173-8 J.-D. Rochaix, M. Goldschmidt-Clermont and S. Merchant (eds.): The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. 1998 ISBN 0-7923-5174-6 H.A. Frank, A.J. Young, G. Britton and R.J. Cogdell (eds.): The Photochemistry of Carotenoids. 1999 ISBN 0-7923-5942-9 R.C. Leegood, T.D. Sharkey and S. von Caemmerer (eds.): Photosynthesis: Physiology and Metabolism. 2000 ISBN 0-7923-6143-1 B. Ke: Photosynthesis: Photobiochemistry and Photobiophysics. 2001 ISBN 0-7923-6334-5 E.-M. Aro and B. Andersson (eds.): Regulation of Photosynthesis. 2001 ISBN 0-7923-6332-9 C.H. Foyer and G. Noctor (eds.): Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism. 2002 ISBN 0-7923-6336-1 B.R. Green and W.W. Parson (eds.): Light-Harvesting Antennas in Photosynthesis. 2003 ISBN 0-7923-6335-3 A.W.D. Larkum, S.E. Douglas and J.A. Raven (eds.): Photosynthesis in Algae. 2003 ISBN 0-7923-6333-7 D. Zannoni (ed.): Respiration in Archaea and Bacteria. Diversity of Prokaryotic Electron Transport Carriers. 2004 ISBN 1-4020-2001-5 D. Zannoni (ed.): Respiration in Archaea and Bacteria. Diversity of Prokaryotic Respiratory Systems. 2004 ISBN 1-4020-2002-3 D. Day, A.H. Millar and J. Whelan (eds.): Plant Mitochondria. From Genome to Function. 2004 ISBN 1-4020-2399-5 Forthcoming.
19. G. Papageorgiou and Govindjee (eds.): Chlorophyll a Fluorescence. A Signature of Photosynthesis. 2004 ISBN 1-4020-3217-X
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