Photosynthesis in Algae

498 Pages·2003·19.038 MB·English

by  Susan E. Douglas, John A. Raven, Anthony W. D. Larkum (auth.), Anthony W. D. Larkum, Susan E. Douglas, John A. Raven (eds.)

Photosynthesis in Algae
Advances in Photosynthesis and Respiration
VOLUME 14
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, Osnabrilck, 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 aII life. Advances in Photosynthesis and Respiration is a book
series that provides a comprehensive and state-of-the-art account of research in photo
synthesis 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 aII growth and
reproduction in these and almost aII other organisms. As such, virtually aII 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 medici ne, 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
an the back cover.
Photosynthesis in Algae
Edited by
Anthony W.D. Larkum
School of Biological Sciences,
University of Sydney, Australia
Susan E. Douglas
National Research Council,
Institute for Marine Biosciences, Canada
and
John A. Raven
Department of Biological Sciences,
University of Dundee, u.K.
Springer-Science+Business Media, BV
A C.I.P. Catalogue record lor this book is available Irom the Library 01 Congress.
ISBN 978-94-010-3772-3 ISBN 978-94-007-1038-2 (eBook)
DOI 10.1007/978-94-007-1038-2
The cover picture is a conlocal scanning microscope picture 01 the gyres 01 chloroplasts in an undescribed species
01 Spirogyra which has "Iri Ils" along the margins. The light areas are putative grana (see Chapter 2). The picture was
taken by Brian Gunning in lalse colour using a Biorad MRC-600 conlocal microscope with a projection 0126 optical
sections imaged at 0.4 micrometre locusing intervals with a 1O Ox Planapo oil-immersion Zeiss lens.
Printed an acid-free paper
AII Rights Reserved
© 2003 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 2003
Softcover reprint of the hardcover 1 st edition 2003
No part 01 this work may be reproduced, stored in a retrieval system, or transmitled
in any lorm or by any means, electronic, mechanical, photocopying, microlilming, recording
or otherwise, without writlen permission Irom the Publisher, with the exception
01 any material supplied specilically lor the purpose 01 being entered
and executed on a computer system, lor exclusive use by the purchaser 01 the work.
Editorial
Advances in Photosynthesis and Respiration
Volume 14: Photosynthesis in Algae
I am extremely delighted to announce the (12) Photosynthetic Nitrogen Assimilation and
publication of the long-awaited Photosynthesis in Associated Carbon and Respiratory Metab
Algae edited by Anthony Larkum, Susan Douglas olism (Christine Foyer and Graham Noctor,
and John Raven. It is Volume 14 in our Series editors,2002); and
AdvancesinPhotosynthesisandRespiration(AIPH) (13) Light HarvestingAntennas (Beverley Green
andisasequeltothepreviousthirteenvolumesinthe and WilliamParson, editors,2003).
series. See <http://www.wkap.nl/series.htrnlAIPH> for
furtherinformationandto orderthesebooks.Please
Published Volumes note that themembersoftheInternationalSocietyof
Photosynthesis Research, ISPR (<http://www.
(1) Molecular BiologyofCyanobacteria (Donald Photosynthesisresearch.org», receive special
R. Bryant, editor, 1994); discounts.
(2) Anoxygenic Photosynthetic Bacteria (Robert
E. Blankenship, MichaelT.Madiganand Carl
E. Bauer, editors, 1995); Photosynthesis in Algae
(3) BiophysicalTechniquesinPhotosynthesis(Jan
Algae are a fascinating group oforganisms, which
Amesz* and ArnoldJ.HoW, editors, 1996);
refuseto be classified. Onemay simplyplacethem
(4) OxygenicPhotosynthesis:TheLightReactions
in the Protists, one ofthe six Kingdoms ofNature.
(DonaldR.artand CharlesF.Yocum, editors,
However this ignores the fact that they arc
1996);
photosynthetic and are undeniably related in some
(5) Photosynthesis andthe Environment (Neil R.
way to the land plants (Plantae). It also places the
Baker, editor, 1996);
algal group, which represents some ofthe largest
(6) Lipids inPhotosynthesis: Structure, Function organismsontheplanetinaKingdomthat istypified
and Genetics (Paul-Andre Siegenthaler and by microscopic unicellular organisms! Ofcourse
NorioMurata, editors, 1998); this has not deterred workers in photosynthesis,
(7) The Molecular Biology ofChloroplasts and almostall ofwhomwill have aflask ortwo ofalgae
MitochondriainChlamydomonas(JeanDavid growingsomewhereintheirlaboratories,eventhough
Roehaix, Michel Goldschmidt-Clermont and they devote their main work to higher plants. As
SabeehaMerchant, editors, 1998); pointedoutinthePrefacetothis volume,italso does
(8) ThePhotochemistryofCarotenoids(HarryA. not prevent frequent sallies into the domain of
Frank, Andrew J.Young, George Britton and Bacteria,tomakeuseofthephotosyntheticproperties
RichardJ.Cogdell, editors, 1999); ofCyanobacteria, even though these organisms are
no longercalled'algae.'
(9) Photosynthesis: Physiology and Metabolism
Weare fortunate in having three outstanding and
(RichardC.Leegood,ThomasD.Sharkeyand
charmingeditorswhoseinterestshave allowedthem
Susannevon Caemmerer,editors,2000);
aclearoverviewofacomplexfield andhas allowed
(10) Photosynthesis:PhotobiochemistryandPhoto
them to choose an excellent set ofauthors out ofa
biophysics(BaconKe, author, 2001);
armyofgreatresearchers inthe field. TonyLarkum
(11) Regulation ofPhotosynthesis (Eva-Mari Aro
isbasicallyaplantphysiologistbuthas workedatall
and BertilAndersson,editors, 2001)
levelsofphotosynthesisfromwholeecosystemssuch
"deceased ascoralreefstogenesforthelight-harvestingproteins
of dinoflagellates and prochlorophytes. Susan research in various areas of photosynthesis and
Douglasisamolecularbiologistwho has sequenced respiration. Photosynthesisisthe processbywhich
cryptophyte genes and most recently took a major higherplants, algae, andcertain species ofbacteria
role in sequencing the three chromosomes of the transform and store solar energy in the form of
relic nucleus (nucleomorph) of the cryptophyte energy-rich organic molecules. These compounds
Guillardia theta. John Raven is an eclectic algal are in turn used as the energy source for all growth
physiologist, whose major contributions have been and reproduction in these and almost all other
in quantifying the roles ofvarious pathways in the organisms. As such, virtually all life on the planet
carbonmetabolismofalgae as well as contributing ultimately depends on photosynthetic energy
prolificallyto discussiononthe evolutionofCyano conversion. Respiration, which occurs in mito
bacteria,algaeand land plants. chondriaandinbacterialmembranes,utilizesenergy
Knowing the editors and the topic ofthe specific presentinorganicmoleculesto fuel awiderange of
volumeare importanttome. Wehave includedbrief metabolic reactions critical for cell growth and
biographies and photographs ofthe editors in this development. In addition, many photosynthetic
volume. My interestin algaedates backto the time organisms engage in energetically wasteful photo
when I was a graduate student ofRobert Emerson respiration that begins in the chloroplast with an
(who himselfwas a student ofOtto Warburg); the oxygenationreactioncatalyzedbythe sameenzyme
greenalga Chlorellawas thechoiceofresearchthen. responsible for capturing carbon dioxide in photo
A1957groupphotographandashamelesslyproduced synthesis. This series of books spans topics from
listing ofsome ofour findings are given following physicstoagronomyandmedicine,fromfemtosecond
this 'Editorial.' Ihave beenfortunate to know Tony (10.15 s) processes to season-longproduction, from
the most. Ihave beenhis guestonceat his pleasant the photophysics of reaction centers, through the
homeinSydneyand enjoyedwithhima'walkinthe electrochemistry ofintermediate electron transfer,
x
ocean' that he led in Heron Island in 2001. The to the physiologyofwholeorganisms, and from
enjoymentofseeingthe marinelife thereandinhis raycrystallographyofproteinstothe morphologyof
laboratory has left an everlasting imprint on my organelles and intact organisms. The intent ofthe
mind. Ihave admiredthework ofSusan,buthaveyet series is to offer beginning researchers, advanced
tomeetherpersonally.However,ImetJohnatUrbana, undergraduatestudents,graduatestudents,and even
Illinois, when he gave an excitinglecturewearinga research specialists, a comprehensive, up-to-date
Scottish kilt. (1have been too 'shy' to ever give a picture ofthe remarkable advances across the full
lecture wearing the Indian 'Kurta-Pajama and the scope of research on bioenergetics and carbon
NehruJacket;Icould,ofcourse,neverweara'Dhoti' metabolism.
for the fear itmay fall down inpublic.)
Thevariouschaptersinthis bookhavebeautifully
coveredthemajoraspectsofphotosynthesisinalgae; Future Books
theyarewrittenbymajorauthoritiesinthefield. Iam
pleased to see inclusion ofdiscussions on Cyano The readersofthe currentseries are encouragedto
bacteria, prochlorophytes (prokaryotes that have watchfor the publicationofthe forthcomingbooks:
chlorophyll b as well as chlorophyll a) and newly (I) RespirationinArcheaandBacteria.2volumes
discovered Acaryochloris marina, which possesses (Editor: DavideZannoni);
chlorophylld.Thisbookwillservegraduatestudents, (2) Chlorophylls and Bacteriochlorophylls:
teachers and researchers in the areas of plant Biochemistry, Biophysics and Biological
physiology,cellularandmolecularbiology,integrative Function(Editors:BernhardGrimm,Robert1.
biology,biochemistry,biophysicsandglobalecology. Porra,WolfhartRudigerandHugo Scheer);
(3) Chlorophyll a Fluorescence: A Signature of
Photosynthesis(Editors:GeorgePapageorgiou
The Scope ofthe Series and Govindjee);
(4) Photosystem II: The Water/Plastoquinone
Advances in Photosynthesis and Respiration is a Oxido-reductase in Photosynthesis (Editors:
book series that provides, at regular intervals, a Thomas1.WydrzynskiandKimiyuki Satoh);
comprehensive and state-of-the-art account of (5) Plant Respiration (Editors: Miquel Ribas-
vi
Carbo andHans Lambers); Respiration; Protonation and ATP Synthesis;
(6) Photosystem I: The NADP+/Ferredoxin FunctionalGenomics;TheCytochromes;Laboratory
Oxidoreductase in Oxygenic Photosynthesis MethodsforStudyingLeavesandWholePlants;and
(Editor: John Golbeck); C-3andC-4 Plants.
(7) Photosynthesis: A Comprehensive Treatise; Readers are requested to send their suggestions
Biochemistry, Biophysics and Molecular fortheseandfuturevolumes(topics, namesoffuture
Biology, 2 volumes (Editors: Julian Eaton editors, and of future authors) to me by E-mail
Ryeand BaishnabTripathy) ([email protected])orfax(1-217-244-7246).
(8) Photoprotection, Photoinhibition, Gene In view of the interdisciplinary character of
RegulationandEnvironment(Editors:Barbara research inphotosynthesis and respiration, it ismy
Demmig-Adams, William W Adams III and earnest hopethatthisseriesofbooks willbeusedin
Autar Mattoo); educating students andresearchersnotonlyinPlant
(9) TheStructureandFunctionofPlastids(Editors: Sciences, Molecular and Cell Biology, Integrative
Kenneth HooberandRobert Wise);and Biology, Biotechnology, Agricultural Sciences,
(l0) History ofPhotosynthesis Research (Editor: Microbiology, Biochemistry, and Biophysics, but
Govindjee) alsoinBioengineering, Chemistry, and Physics.
In addition to these contracted books, we are I take this opportunity to thank Tony Larkum,
interestedinpublishing several other books.Topics SusanDouglas,JohnRaven,alltheauthorsofvolume
underconsiderationare:MolecularBiologyofStress 14,Larry Orr,Jacco Flipsen, Noeline Gibson, Evan
in Plants; Global Aspects of Photosynthesis and Delucia, and my wife Rajni Govindjee for their
Respiration; Protein Complexes ofPhotosynthesis valuablehelpandsupportthatmade thepublication
and Respiration; Biochemistry and Biophysics of ofPhotosynthesis inAlgae possible.
August 15,2003
Govindjee
Series Editor
Advances inPhotosynthesisandRespiration
UniversityofIllinois atUrbana-Champaign
DepartmentofPlant Biology
265MorrillHall, 505 South GoodwinAvenue
Urbana, IL61801-3707,U.S.A.
E-mail: [email protected];
URL: http://www.1ife.uiuc.edu/govindjee
VII
A 1957photographofGovindjee(3rdfromtheright,holdingoneoftheLavorels' children), Robert Emerson(151ontheleft,holding
anotherchildoftheLavorels),andRuthV.Chalmers(Emerson'sassistant;)Cdfromtheleft).Othersinthephotoare:MadameMary-Jo
Lavorel(2ndfromleft),JeanLavorel(5thfromleft)andPaulLatimer(extremeright).
Govindjee
Govindjeewastrainedinphycology,duringhisM.Sc. Anacystis, (1967, 1968; G.Papageorgiou); and in
course (1952-1954), by Professor A.K. Mittra of Chiarella (1970; J-M. Briantais); temperature
AllahabadUniversity,India.From1956-1958,Robert dependence ofChia fluorescencebandsat685nm,
Emerson and his assistant Ruth V. Chalmers gave 696nm,andat730nm,downto4K,suggestingthat
excellenttrainingintheculture,growth,maintenance, Forster energy transfer is the most probable
and physiology of various algae. This included mechanismofenergy transfer inalgae(1966-1970;
quantum yield measurements ofoxygen evolution F. Cho);slowChiafluorescence changes related to
by Emerson's most precise differential two-vessel photophosphorylation and other non-Q;-related
manometry(usingacathetometertoreadthepressure events(1967-1972;G. Papageorgiou,P. Mohanty);
changesassmallas0.0Imm, while the manometer maximum quantum yield ofoxygen evolutiondoes
wasshaking).Aninteresting thingabout Emerson's notexceed0.12eveninyoungsynchronouslygrown
manometerwasthat itused a low-density,but foul Chiarella,inthepresenceofcatalyticbluelightand
smelling iso-caproic acid as the manometer fluid! 10% CO i.e., under O. Warburg's experimental
2,
Govindjee's early research included the usc of the conditions (1968; R.Govindjee); existence of a
green alga Chiarella pyrenoidosa, the cyano circadianrhythminChiafluorescence inGonyaulax
bacterium Anacystis nidulans (then called a blue polyedra (1979;B.Sweeney andB.Prezelin); heat
green alga), Navicula minima (a diatom), and inducesstatechanges(1984;P.V.Sane);bicarbonate!
Porphyridium cruentum(ared alga). Laterresearch formate binding near D1-R257 regulates electron
included the use of wild type and several Photo transfer in PSII (1996-1998); elucidating the
system II (PS II) mutants of the cyanobacterium polyphasic rise kinetics ofChi a fluorescence rise
Synechocystis PCC 6803 (now fully sequenced: and the coining ofthe name the OJIP curve (1992
www.kazusa.or.jp!cyanobase!). and the wild type 1995;R.Strasserandhiscoworkers);demonstrating
and several PSII and xanthophyll cycle mutants of thatimagingofthelifetime ofChia fluorescenceis
anothergreenalgaChlamydomonasreinhardtii.The a great tool for measuring quantum yield of
following are some of his, and co-worker's, fluorescence, and, thus of photosynthesis even in
observations:chlorophyll(Chi)a-670isapartofthe single cells of algae (2000-2003; O. Holub,
short-wave photosystem (now called Photosystem M.Seufferheld and R. Clegg);exposure ofcells to
II)inChiarellaandNavicula(1960;E.Rabinowiteh); forced light oscillations suggestsunique regulation
existence of a two-light effect through Chi a ofattachmentandde-attachment ofphycobi1isomes
fluorescence measurements (1960; S. Ichimura); to PSII core Chi a-containing protein complexes
existenceofapigment withabsorptionat750nmin (2003; L. Nedbal). SeeVolume 12ofAIPH Series
Anacystis (1961; C.Cederstrand); existence of a (Editors:C.FoyerandG.Noctor)forabriefbiography,
newemissionbandinthe692-695nmregionatroom Volume13(Editors:B.GreenandW Parson)forthe
temperature, when photosynthesis is saturated, or story of his name, and http://www.life.uiuc.edu/
blocked, in Porphyridium (1963; A. Krey); in govindjee!forhispublications.
Vlll
Contents
Editorial v
Contents ix
Preface xvi
Color Plates CP-1
Introductory Chapters
1 The Algae and their General Characteristics 1-10
Susan E. Douglas, John A. Raven andAnthony W. D. Larkum
Summary 1
I. Introduction 2
II. The Algae:TheirOriginsand Diversity 2
III. The Green, Redand BrownAlgae 4
IV. The Chromophytes 4
V. TheChlorarachniophytes 7
VI. The Euglenophytes 7
VII. AlgalGenomes 7
VIII.AlgaeasSourcesofNaturalProducts 8
IX. Concluding Remarks 8
Acknowledgements 9
References 9
2 Algal Plastids:Their FineStructure and Properties 11-28
Anthony W. D. Larkum andMaret Vesk
Summary 11
I. Introduction 12
II. OriginofPlastids 12
III. Chlorophyte Plastids 13
IV. RhodophytePlastids 16
V. Cyanelles (Glaucocystophyte Plastids) 18
VI. Cryptophyte Plastids 18
VII. Chlorarachniophyte Plastids 20
VIII.Euglenophyte Plastids 20
IX. Dinoflagellate Plastids 20
X. Chrysophyte (Ochrophyte) Plastids 22
XI. Phaeophyte,Bacillariophyte,Eustigmatophyte, Raphidophyte, Synurophyte,
Pelagophyte,Silicoflagellate, Pedinellidand Xanthophyte Plastids 23
XII. Haptophyte Plastids 23
IX
XIII.Apicomplexan Plastids 24
XIV.Kleptoplastids 24
XV. Microstructure oftheThylakoid Membrane 24
Acknowledgments 26
References 26
3 The Photosynthetic Apparatus of ChlorophyllJrand d-Containing
Oxyphotobacteria 29-62
Frederic PertenskyandLaurence Garczarek
Summary 29
I. Introduction 30
II. Advances inPhotosynthesisinChlorophyll b- and d-Containing
Oxyphotobacteria 32
III. Green Oxyphotobacteriaandthe EndosymbioticTheory ofGreen
PlastidsEvolution 51
IV. Concluding Remarks 55
Acknowledgments 56
References 56
Molecular Genetics ofAlgae
4 Structure and Regulationof Algal Light-Harvesting Complex Genes 63-82
Dion G.Durnford
Summary 63
I. Introduction 64
II. HigherPlantLight-HarvestingComplexes 64
III. Algal Light-HarvestingComplexes 67
IV. Origin andEvolutionofthe Light-HarvestingAntennae 76
V. Concluding Remarks 77
Acknowledgments 77
References 77
5 Functional Analysis of PlastidGenesthrough Chloroplast Reverse
Genetics in Chlamydomonas 83-94
Jean-David Rochaix
Summary 83
I. Introduction 84
II. Algal ChloroplastTransformation 84
III. ReverseChloroplastGeneticsofPhotosynthesis 85
IV. SeveralyefsEncodeNovelProteinsInvolvedinPhotosynthesis 87
V. Chloroplast ReverseGeneticsofEssentialGenesof Chlamydomonas 89
VI. Conclusions and Prospects 92
Acknowledgments 92
References 92
x