<<

Photosynthesis in Algae Advances in 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 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 , algae, and certain species of bacteria transform and store in the form of energy-rich organic molecules. These compounds are in turn used as the energy source for aII growth and in these and almost aII other . 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 growth and development. In addition, many photosynthetic organisms engage in energetically wasteful that begins in the with an oxygenation reaction catalyzed by the same enzyme responsible for capturing in photosynthesis. This series of books spans topics from physics to 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 to the 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 in an undescribed species 01 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 1OOx Planapo -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 Advances in Photosynthesis andRespiration (AIPH) (13) Light Harvesting Antennas (Beverley Green and is a sequel to the previous thirteen volumes in the and William Parson, editors, 2003). series. See for further information and to order these books. Please Published Volumes note that the members ofthe International Society of Photosynthesis Research, ISPR (

vi Carbo and Hans Lambers); Respiration; Protonation and ATP Synthesis; (6) : The NADP+/Ferredoxin Functional Genomics; The Cytochromes; Laboratory Oxidoreductase in Oxygenic Photosynthesis Methods for Studying and Whole Plants; and (Editor: John Golbeck); C-3 and C-4 Plants. (7) Photosynthesis: A Comprehensive Treatise; Readers are requested to send their suggestions Biochemistry, Biophysics and Molecular for these and future volumes (topics, names offuture Biology, 2 volumes (Editors: Julian Eaton• editors, and of future authors) to me by E-mail Rye and Baishnab Tripathy) ([email protected]) or fax (1-217-244-7246). (8) Photoprotection, , Gene In view of the interdisciplinary character of Regulation and Environment (Editors: Barbara research in photosynthesis and respiration, it is my Demmig-Adams, William W Adams III and earnest hope that this series ofbooks will be used in Autar Mattoo); educating students and researchers not only in Plant (9) TheStructureandFunctionofPlastids (Editors: Sciences, Molecular and , Integrative Kenneth Hoober and Robert Wise); and Biology, , Agricultural Sciences, (l0) History ofPhotosynthesis Research (Editor: , Biochemistry, and Biophysics, but Govindjee) also in Bioengineering, Chemistry, and Physics. In addition to these contracted books, we are I take this opportunity to thank Tony Larkum, interested in publishing several other books. Topics Susan Douglas, John Raven, all the authors ofvolume under consideration are: Molecular Biology of Stress 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 of Photosynthesis valuable help and support that made the publication and Respiration; Biochemistry and Biophysics of ofPhotosynthesis in Algae possible.

August 15,2003

Govindjee Series Editor Advances in Photosynthesis and Respiration University ofIllinois at Urbana-Champaign Department of Plant Biology 265 Morrill Hall, 505 South Goodwin Avenue Urbana, IL 61801-3707, U.S.A. E-mail: [email protected]; URL: http://www.1ife.uiuc.edu/govindjee

VII A 1957 photograph of Govindjee (3rd from the right, holding one of the Lavorels' children), Robert Emerson (151 on the left, holding another child ofthe Lavorels), and Ruth V. Chalmers (Emerson's assistant; )Cd from the left). Others in the photo are: Madame Mary-Jo Lavorel (2nd from left), Jean Lavorel (5th from left) and Paul Latimer (extreme right).

Govindjee

Govindjee was trained in , during his M.Sc. Anacystis, (1967, 1968; G. Papageorgiou); and in course (1952-1954), by Professor A.K. Mittra of Chiarella (1970; J-M . Briantais); temperature Allahabad University, India. From 1956-1958, Robert dependence ofChi a fluorescence bands at 685 nm, Emerson and his assistant Ruth V. Chalmers gave 696 nm, and at 730 nm, down to 4 K, suggesting that excellent training in the culture, growth,maintenance, Forster energy transfer is the most probable and physiology of various algae. This included mechanism ofenergy transfer in algae (1966-1970; quantum yield measurements of evolution F. Cho); slow Chi a fluorescence changes related to by Emerson 's most precise differential two-vessel photophosphorylation and other non-Q; -related manometry (using a cathetometerto read the pressure events (1967-1972; G. Papageorgiou , P. Mohanty) ; changes as small as 0.0 I mm, while the manometer maximum quantum yield of oxygen evolution does was shaking). An interesting thing about Emerson 's not exceed 0.12 even in young synchronously grown manomete r was that it used a low-density, but foul• Chiarella, in the presence ofcatalytic light and smelling iso-caproic acid as the manometer fluid! 10% CO2, i.e., under O. Warburg's experimental Govindjee's early research included the usc of the conditions (1968; R. Govindjee); existence of a green alga Chiarella pyrenoidosa, the cyano• circadian rhythm in Chi a fluorescence in Gonyaulax bacterium Anacystis nidulans (then called a blue• polyedra (1979; B. Sweeney and B. Prezelin); heat• green alga), minima (a ), and induces state changes (1984; P.V. Sane); bicarbonate! Porphyridium cruentum (a red alga). Later research 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 of Chi a fluorescence rise Synechocystis PCC 6803 (now fully sequenced : and the coining of the name the OJIP curve (1992• www.kazusa.or.jp!cyanobase!). and the wild type 1995; R. Strasser and his coworkers); demonstrating and several PSII and xanthophyll cycle mutants of that imaging ofthe lifetime ofChi a fluorescence is another green alga Chlamydomonas reinhardtii.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-670 is a part ofthe single cells of algae (2000-2003; O. Holub, short-wave photosystem (now called Photosystem M. Seufferheld and R. Clegg); exposure of cells to II) in Chiarella and Navicula (1960; E. Rabinowiteh); forced light oscillations suggests unique regulation existence of a two-light effe ct through Chi a ofattachment and de-attachment ofphycobi1isomes fluorescence measurements (1960; S. Ichimura) ; to PSII core Chi a-containing protein complexes existence ofa with absorption at 750 nm in (2003; L. Nedbal). See Volume 12 ofAIPH Series Anacystis (1961; C. Cederstrand); existence of a (Editors:C. Foyer and G.Noctor) fora briefbiography, new emission band in the 692-695 nm region at room Volume 13 (Editors: B. Green and W Parson) for the temperature, when photosynthesis is saturated, or story of his name, and http://www.life.uiuc.edu/ blocked, in Porphyridium (1963 ; A. Krey); in govindjee! for his publications.

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 and Anthony W. D. Larkum Summary 1 I. Introduction 2 II. The Algae: Their Origins and Diversity 2 III. The Green, Red and 4 IV. The Chromophytes 4 V. The 7 VI. The Euglenophytes 7 VII. Algal Genomes 7 VIII. Algae as Sources of Natural Products 8 IX. Concluding Remarks 8 Acknowledgements 9 References 9

2 Algal : Their Fine Structure and Properties 11-28 Anthony W. D. Larkum and Maret Vesk Summary 11 I. Introduction 12 II. Origin of Plastids 12 III. Chlorophyte Plastids 13 IV. Rhodophyte Plastids 16 V. Cyanelles (Glaucocystophyte Plastids) 18 VI. Cryptophyte Plastids 18 VII. Plastids 20 VIII. Euglenophyte Plastids 20 IX. Plastids 20 X. Chrysophyte (Ochrophyte) Plastids 22 XI. Phaeophyte, Bacillariophyte, , , Synurophyte, Pelagophyte, Silicoflagellate, Pedinellid and Xanthophyte Plastids 23 XII. Plastids 23

IX XIII. Apicomplexan Plastids 24 XIV. Kleptoplastids 24 XV. Microstructure of the Thylakoid Membrane 24 Acknowledgments 26 References 26

3 The Photosynthetic Apparatus of Chlorophyll Jr and d-Containing Oxyphotobacteria 29-62 Frederic Pertensky and Laurence Garczarek Summary 29 I. Introduction 30 II. Advances in Photosynthesis in Chlorophyll b- and d-Containing Oxyphotobacteria 32 III. Green Oxyphotobacteria and the Endosymbiotic Theory of Green Plastids Evolution 51 IV. Concluding Remarks 55 Acknowledgments 56 References 56

Molecular Genetics ofAlgae

4 Structure and Regulation of Algal Light-Harvesting Complex Genes 63-82 Dion G. Durnford

Summary 63 I. Introduction 64 II. Higher Plant Light-Harvesting Complexes 64 III. Algal Light-Harvesting Complexes 67 IV. Origin and Evolution of the Light-Harvesting Antennae 76 V. Concluding Remarks 77 Acknowledgments 77 References 77

5 Functional Analysis of Genes through Chloroplast Reverse Genetics in Chlamydomonas 83-94 Jean-David Rochaix Summary 83 I. Introduction 84 II. Algal Chloroplast Transformation 84 III. Reverse Chloroplast Genetics of Photosynthesis 85 IV. Several yefs Encode Novel Proteins Involved in Photosynthesis 87 V. Chloroplast Reverse Genetics of Essential Genes of Chlamydomonas 89 VI. Conclusions and Prospects 92 Acknowledgments 92 References 92

x 6 Biochemistry and Regulation of Chlorophyll Biosynthesis 95-131 A. Bruce Cahoon and Michael P. Timko Summary 96 I. Introduction 96 II. An Overview of Tetrapyrroles and Their Derivatives 96 III. Chlorophyll Forms and Their Distribution in Algal Species 98 IV. Early Steps in Chlorophyll Biosynthesis 98 V. The Pathway from ALA to Protoporphyrin IX 102 VI. The Branch 107 VII. The Branch-Chlorophyll a Formation 108 VIII. Biosynthesis of Chlorophyll b and Other Algal Chlorophylls 119 Acknowledgments 122 References 122 Summary 133

Biochemistry and Physiology ofAlgae

7 Oxygenic Photosynthesis in Algae and Cyanobacteria: Electron Transfer in Photosystems I and II 133-156 Jonathan H. A. Nugent, Saul Purton and Michael C. W. Evans Summary 133 I. Introduction 134 II. Overview of Photosystems I and II 134 III. Mutagenesis and Genetic Engineering of the Photosystems 135 IV. Photosystem II Function 139 V. Photosystem II Structure 143 VI. Photosystem I 146 VII. Conclusions 151 Acknowledgment 151 References 151

8 Oxygen Consumption: Photorespiration and Chlororespiration 157-181 John Beardall, Antonietta Quigg and John A. Raven Summary 158 I. Introduction 158 II. Photorespiration 159 III. Chlororespiration: A Mechanism to Maintain Thylakoid Membrane Energization in the Dark? 168 Acknowledgments 178 References 179

9 The Water-Water Cycle in Algae 183-204 Chikahiro Miyake and Kozi Asada Summary 184 I. Introduction 184 II. The Water-Water Cycle in Plant Chloroplasts 185

xi III. Operation of the Water-Water Cycle in Cyanobacteria and Eukaryotic Algae 189 IV. Scavenging System of 02- and HP2 in the Algal Water-Water Cycle 190 V. Physiological Functions of the Water-Water Cycle in Cyanobacteria and Eukaryotic Algae 196 VI. Concluding Remarks 197 Acknowledgment 198 References 198

10 Carbohydrate Metabolism and Respiration in Algae 205-224 John A Raven and John Beardall Summary 205 I. Introduction 206 II. Carbohydrate Metabolism: Low M, Compounds 207 III. Carbohydrate Metabolism: Storage 208 IV. Carbohydrate Metabolism: Structural Polysaccharides 209 V. Respiration: Carbon Pathways 211 VI. Respiration: Redox Reactions and Energy Conservation 213 VII. Respiration: Spatial and Temporal Aspects 218 VIII. Quantifying Carbohydrate Metabolism and Respiration in Relation to Growth and Maintenance 220 Acknowledgments 221 References 221

11 Carbon Acquisition Mechanisms of Algae: Carbon Dioxide Diffusion and Carbon Dioxide Concentrating Mechanisms 225-244 John A Raven and John Beardall Summary 226 I. Introduction 226 II. Rubisco Kinetic Properties in Relation to the CO2and 02 Concentrations in Cyanobacterial and Algal 226 III. Lines of Evidence Used in Distinguishing Organisms Relying on Diffusive CO2 Entry from Those Using Carbon Concentrating Mechanisms (CCMs) 229 IV. Occurrence and Mechanism of CCMs 230 V. Evolution of CCMs 240 VI. Conclusions and Prospects 240 Acknowledgments 241 References 241

Light-Harvesting Systems in Algae

12 Modeling the Excitation Energy Capture inThylakoid Membranes 245-276 Hans-Wilhelm Trissl Summary 246 I. Introduction 246 II. Structural Composition of the Thylakoid Membrane 247 III. Experimental Approaches 253 IV. Kinetic Modeling of the Thylakoid Membrane 256

Xll V. Concluding Remarks 271 Acknowledgments 271 References 272

13 Light-Harvesting Systems in Algae 277-304 Anthony W. D. Larkum Summary 278 I. Introduction 278 II. Chlorophylls 279 III. Light-Harvesting Proteins 283 IV. Optimizing Light-Harvesting Architecture 285 V. Problems with Photosystem II 287 VI. Off-Loading Excess Light Energy: Xanthophyll Cycle and Reaction Center Sinks 288 VII. Control of Light Harvesting 291 Acknowledgments 299 References 299

14 Red, and Glaucocystophyte Algal Phycobiliproteins 305-334 Colleen Mary Toole and F. C. Thomas Allnutt Summary 306 I. Introduction 306 II. Structure and Components of 307 III. Molecular Biology of Red Algal, Glaucocystophyte and Cryptomonad Phycobiliproteins 310 IV. Phycobiliprotein Structure 311 V. Phycobiliprotein Types 315 VI. Phycobiliprotein Crystal Structure 319 VII. Bilin Chromophores 322 VIII. Energy Transfer 326 IX. Applications/Industrial Uses 328 References 329

15 of Light Harvesting Systems: Energy Transfer Processes from Fucoxanthin and Peridinin to Chlorophyll 335-349 Mamoru Mimuro and Seiji Akimoto Summary 335 I. Introduction 336 II. Distribution of Carotenoids in Algae 336 III. Optical Properties of Carotenoids in Relation to Functions 337 IV. Functions 343 V. Antenna Function of Carotenoids in Algae 344 VI. Electronic States and Dynamic Properties of Molecules 345 VII. Energy Transfer Processes and Mechanism 346 References 348

xiii General Aspects of Photosynthesis in Algae

16 Photoinhibition, UV-B and Algal Photosynthesis 351-384 Linda A. Franklin, C. Barry Osmond and Anthony W. D. Larkum Summary 352 I. Introduction 352 II. The Algal Light Climate 354 II. Photoinhibition by PAR 357 III. Effects of UV Radiation 364 IV. Photoinhibition and UV Stress in the Field 371 V. Scope for Further Research 373 Acknowledgment 375 References 375

17 Adaptation, Acclimation and Regulation in Algal Photosynthesis 385-412 John A. Raven and Richard J. Geider Summary 386 I. Introduction 386 II. The Range of Resource Availabilities and Other Environmental Factors within Which Algae Can Photosynthesize 389 III. Adaptation of the Photosynthetic Apparatus 390 V. Adaptation of Algal Photosynthesis to Environmental Extremes 396 VI. Acclimation of Algal Photosynthesis 400 VII. Regulation of Algal Photosynthesis 406 VIII. Rates of Regulation and Acclimation 407 IX. Con~u~ons 408 Acknowledgments 409 References 409

18 Photosynthesis in Marine Macroalgae 413-435 D. Hanelt, C. Wieneke and K. Bischof Summary 413 I. Introduction 414 II. Radiation Conditions in Coastal 415 III. Light Absorption by Macroalgae 417 IV. Determination of Photosynthetic Rates 418 V. Effects of Excessive Light on Photosynthesis 423 VI. Algal Photosynthesis Under Low Light Conditions 427 VII. Seasonal Photosynthetic Performance of Macroalgae 427 VIII. Adaptation and Acclimation of Photosynthesis and Respiration to Temperature and Salinity 428 References 429

19 Photosynthesis in Symbiotic Algae 437-455 David Yellowlees and Mark Warner Summary 437

XIV I. Introduction 438 II. Algal Symbiotic Associations 439 III. The Host-Algal Interface 439 IV. Carbon Acquisition, Fixation and 440 V. Photoacclimation and Photoadaptation 446 VI. and Photoinhibition 447 References 450

Index 457

xv xvii xviii xix xx Color Plates

-

Color Plate I. A. Colonies ofthe green volvocalean alga . Scale bar, 30 Jlffi. B. A ofthe red alga La urencia intrica ta. Scale bar, I em. C. Part of a thallus of the brown alga , Scale bar, I cm. D. The cryptomonad Cryptomonas sp. under the light microscope. The several plastids in each cell are readily seen. The two equal Ilagella are not so easily seen under the light microscope. Scale bar, 2Jlffi. Photography by M Ricketts. See Chapter I, p. 4.

Anthony W. Larkum, Susan E. Douglas and John A. Raven (eds): Photosynth esis in Algae, pp.CP1- CP.J. © 2003 Kluwer Academic Publishers. Printed in The Netherlands. Color Plates

Color Plate 2. Confoc al images of chlorophyll fluorescence in various ehlorophytes. A. Oedogonium (species unknown, local collection) ; x3,300 . B. Cladophora (specie s unknown, local collect ion); x2,800. C. Spirogyra (species unknown , local collection) x31O. C.(Inset) Spirogyra as in C. at x 3000. D. Klebsormidium flaccidum (UTEX #LB2017) X2,300. E Nitella translucens (Wasteneys collection) X24000. All scale bars S lim except low magnification ofSpirogyra which is 100 J.1m .Micrographs kindly provided by Brian Gunnin g: for further details and descriptions, see Gunning and Schwartz, 1999. See Chapter 2, p. 17 .

CP-2 o 0"~ "'U f[ CD lJl

6"-0 l& ',>- ',>- ~ ~n'" '- ",3o\le\en'e "'3o\le\en'b\\\, n'"

o "'0 I \;.)

v' v' l& 6S0

',>- ~n'" ",a-"e\en'e

Color Plate 3, Time-resolved emission spectra (TRES) oft he thylakoid membrane of Ostreobium sp. as caleulatcd with the reaction scheme of Fig. 8 (p. 265), The TRES arc depicted for two different excitation wavelengths and two different time scales as indicated. See Chapter 12, p. 265. Color Plates

A. B.

,) 7. K L C

~ l-al 1oop

ApeB ubunit of monomer 2

Color Plate 4. Structure of the small APC linker polypeptide (Ll 8) and its interactions with surrounding central phyco cyanobilin chromophores covalently attached to allophycocya nin monomers I and 2. Panel A) Structure ofthc Ll 8polypept ide, showing a-helices a l and a2 and three l3-sheets, 13 1, 132 and 133 . The Tyr37 residue, located on a -helix2, is depicted as space-filled atoms. The linker polypeptide is shown as a ribbon structure and colored cyan. Panel B) The same three-dimensional structure ofthe Ll 8 linker polypeptide (cyan) is shown along with its interactions with central phycocyanobilins (PCB) attached to Cys82 residues on allophycocyanin monomers I and 2. The PCBs ofmonomers I and 2 are colored blue and shown as stick figures. Residue Tyr37 located in a-helix2 of the linker polypeptide is shown as space-filled atoms, as is residue Tyr87 of thc ApcB subunit ofmonomer 2. The interact ion of Tyr37 (red) with Tyr8 7 (green) results in a conformational change between monomer 2 and its chromophore, specifically where ring B of PCB is forced in the opposite direction ofTyr87. This interaction is not found in the remain ing two monomers of the APC trimer . Structures were generat ed using Rasmol and the PDB coord inates for APCLc7.8 from the phycob ilisomes of Mastigocladus laminosus (Reuter et al., 1999). See Chapter 14, p. 320.

CPA