Photosynthesis: Photobiochemistry and Photobiophysics

783 Pages·2003·69.744 MB·English

by  Bacon Ke (auth.)

Photosynthesis
Photobiochemistry and Photobiophysics
Advances in Photosynthesis
VOLUME 10
Series Editor:
GOVINDJEE
University of Illinois, Urbana, Illinois, U.S.A.
Consulting Editors:
Jan AMESZ,Leiden, The Netherlands
Eva-Mari ARO,Turku, Finland
James BARBER, London, United Kingdom
Robert E. BLANKENSHIP, Tempe, Arizona, U.S.A.
Norio MURATA, Okazaki, Japan
Donald R. ORT, Urbana, Illinois, U.S.A.
Advances in Photosynthesis is an ambitious book series seeking to provide a compre-
hensive and state-of-the-art account of photosynthesis research. 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 organisms.
As such, virtually all life on the planet ultimately depends on photosynthetic energy con-
version. This series of books spans topics from physics to agronomy, from femtosecond
reactions to season long production, from the photophysics of reaction centers to the
physiology of whole organisms, and from X-ray crystallography of proteins to the morp-
hology of intact plants. The intent of this series of publications is to offer beginning re-
searchers, advanced undergraduate students, graduate students, and even research
specialists a comprehensive current picture of the remarkable advances across the full
scope of photosynthesis research.
The titles published in this series are listed at the end of this volume and those of forthcoming
volumes on the back cover.
Photosynthesis
Photobiochemistry and Photobiophysics
Bacon Ke
Walnut Creek, CA, U.S.A.
KLUWER ACADEMIC PUBLISHERS
NEW YORK,BOSTON, DORDRECHT, LONDON, MOSCOW
eBookISBN: 0-306-48136-7
Print ISBN: 0-7923-6334-5
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To Keiko
Editorial: Advances in Photosynthesis and Respiration
I grew up in the world of photosynthesis. My studies in the field began in 1953, when I was a Master’s
of Science student in Shri Ranjan’s class at Allahabad University, India. Ranjan had not only worked in
the laboratory of F. F. Blackman, which is known for the law of limiting reactions in photosynthesis, but
had also done research in respiration. At that time, I read Volume I (published in 1945) and the first part
of Volume II (published in 1951) of Eugene Rabinowitch’s masterpiece, Photosynthesis and Related
Processes. It was only after 1957, when I came to the University of Illinois at Urbana-Champaign to
work with Robert Emerson, that I read the rest of the masterpiece – Volume II, part 2 (1956). This book
(2088 pages long) made a tremendousimpact on the research of many. Today, it would be impossible for
one author to write a comparable, in-depth book covering all aspects of photosynthesis –the subject has
grown too complex. Between 1990 and 2000, according to Current Contents, 11,576 papers were pub-
lished on photosynthesis. Of those, 3,796 were on photosystem II; 1,059 on photosystem I, 2,044 on
chlorophylla fluorescence, 1,270 on ATP synthase; 1,435 on oxygen evolution, and 1,050 on RIBISCO.
Further, a search onthe Internet through <http://www.google.com>turned up 106,000 on photosynthe-
sis, 8,190 hits on photosystem II, 8,290 hits on chlorophyll fluorescence, 17,400 hits on ATP synthase,
and 5,550 on RUBISCO. Wow!
In the early 1990s, I initiated the series “Advances in Photosynthesis” with Kluwer Academic Pub-
lishers. My earlier experience in writing and editing books (“Photosynthesis” with E. Rabinowitch, John
Wiley & Sons, 1969; “Bioenergetics of Photosynthesis,” 1975; “Photosynthesis,” Vols. I and II, 1982;
and “Light Emission by Plants and Bacteria,” co-edited with Jan Amesz and Dave Fork, 1986; Aca-
demic Press) was of great help in this new endeavor. An earlier series entitled “Topics in Photosynthe-
sis,” edited by J. Barber (Elsevier, the Netherlands), 1976 to early 1990s, had already pioneered the
practice of multi-authored books in photosynthesis. Although “Advances in Photosynthesis”was launched
before this earlierseries had ended, both series proved valuable in this rapidly expanding field.
With the help of Larry Orr at Arizona State University, Tempe, and the assistance of Ad Plaizier,
Gilles Jonker,Natasha Bonnevalle, Jacco Flipsen, and Gloria Verhey at Kluwer Academic Publishers,
we have published the following nine books in the “Advances in Photosynthesis” series.
(1) Molecular Biology ofCyanobacteria (D. A. Bryant, editor, 1994);
(2) Anoxygenic PhotosyntheticBacteria(R. E. Blankenship, M. T. Madigan and C. E. Bauer, editors,
1995);
(3) Biophysical Techniques in Photosynthesis (J. Amesz and A. J. Hoff, editors, 1996);
(4) Oxygenic Photosynthesis: The Light Reactions (D. R. Ort and C. F. Yocum, editors, 1996);
(5) Photosynthesis and the Environment (N. R. Baker, editor, 1996);
(6) Lipids in Photosynthesis: Structure, Function and Genetics (P.-A. Siegenthaler and N. Murata, edi-
tors, 1998);
(7) The Molecular Biology ofChloroplasts and Mitochondria in Chlamydomonas (J-D. Rochaix, M.
Goldschmidt-Clermont and SabeehaMerchant, editors, 1998);
(8) The Photochemistry of Carotenoids (H. A. Frank, A. J. Young, G. Britton and R. J. Cogdell, editors,
1999); and
(9) Photosynthesis: Physiology and Metabolism (R. C. Leegood, T. D. Sharkey and Susanne
von Caemmerer, editors, 2000).
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See <http://www.wkap.nl/series.html/AIPH> for further information and to order these books. Please
note that members of the International Society of Photosynthesis Research, ISPR (<http://www. Pho-
tosynthesis research.org>) receive special discounts.
Although I continue to believe in the value of multi-authored books in this series, I decided that this
precedent could be broken when I discovered that Bacon Ke had written a marvelous manuscript on
photosynthesis in the tradition of Eugene Rabinowitch. I have read Ke’s work, “Photosynthesis:
Photobiochemistry and Photobiophysics,”and believe it to be an important addition to the “Advances in
Photosynthesis” series. Through this book I have learned to appreciate how the kinetics of various reac-
tions, measured by difference absorption spectroscopy and by electron spin resonance, have led to the
current understanding of the pathway of electron transport in both plant and bacterial photosynthesis.
Bacon has woven into the book the atomic structure of the various protein complexes with their function,
in both a scientific and artistic manner, making it unique in dealing with the biochemistry and biophysics
of plant, cyanobacterial, algal, and bacterial photosynthesis. In telling the story of photosynthesis, Bacon
has dealt with the time sequence of reactions from picoseconds to milliseconds in a beautiful manner.
Using the scale = -log(time in seconds), from Martin Kamen’s 1963 book), Bacon has mostly
covered the decades from 12 (picosecond) to 3 (millisecond). This book will be considered a classic in
its field and will serve all beginning students and researchers in the area of the light reactions of photo-
synthesis, up to the production of NADH or NADPH and ATP. It is the first book in the “Advances in
Photosynthesis” series that can be used as a text book in a graduate or upper division undergraduate
course on photosynthesis; we will only need to supplement it with a book on the dark reactions, such as
volume 9 of the series, to cover the entire range of photosynthesis. This great book by Bacon Ke is
volume 10 in the “Advances in Photosynthesis” series. The format of this single-authored book is inten-
tionally different from the previous nine multi-authored books. We hope to continue using both formats
in the future.
In Volume 11, we will make several important changes to the series. The topic of “Respiration” will
be added, and, thus, the title of the series will be changed to “Advances in Photosynthesis and Respira-
tion.” We will also have a new board of consulting editors. Outgoing editors Jan Amesz, The Nether-
lands; Eva-Mari Aro, Finland; James Barber, UK; Robert E. Blankenship, USA; Norio Murata, Japan;
and Donald R. Ort, USA, will be replaced in volume 11 by Eva-Mari Aro, Finland; Christine Foyer, UK;
Elisabeth Gantt, USA; John H. Golbeck, USA; Susan Golden, USA; Wolfgang Junge, Germany; Hartmut
Michel, Germany; and Kimiyuki Satoh, Japan. Eva-Mari Aro (Finland), who joined us only in Vol. 3,
has graciously agreed to serve till Vol. 12, when a new member in the area of respiration will be ap-
pointed. William Ogren served on the board of consulting editors for volume 1. I am particularly thank-
ful to Jan Amesz, Eva-Mari Aro, Bob Blankenship, Norio Murata, and Don Ort for taking an active role
in editing the various volumes in the series. Further, the following new members havealready agreed to
editfuture volumes: Christine Foyer, John Golbeck, Wolfgang Junge, and Kimiyuki Satoh. I thank all
the outgoing consulting board members, the pasteditors and the authors, and welcome all the incoming
board members, the editors and the authors of the future volumes. I would also like to thank Prasanna
Mohanty for making many suggestions for both the current and future book series. Prasanna has also
written detailed reviews of our books in severalIndian journals, bringing information to the photosyn-
thesis community in the developing world. It is my dream that some day we will increase the access to
these books by producing a version that all graduate students throughout the World can afford to pur-
chase.
viii
The future scope of our series will reflect the recognition that photosynthesis and respiration are
intertwined with respect to both the proteincomplexesinvolved and to the entire bioenergeticmachinery
of all life. “Advances in Photosynthesis and Respiration” will be a book series providing a comprehen-
sive 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-richorganicmolecules.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 organisms, and from X-ray crystallography of proteins to
the morphology of organelles and intact organisms. The intent of the series is to offer beginning re-
searchers, graduate students, advanced undergraduate students, and even research specialists, a compre-
hensive, up-to-date picture of the remarkable advances across the full scope of research on bioenergetics
and carbon metabolism.
The readers of the current series are encouraged to watch for the forthcoming books:
(1) Regulatory Aspects of Photosynthesis (volume 11; Editors: E.-M. Aro and B. Andersson);
(2) Light-harvesting Antennas in Photosynthesis (Editors: B. R. Green and W. W. Parson);
(3) Photosynthesis in Algae (Editors: A. W. D. Larkum, S. Douglas, and J. A. Raven);
(4) Photosynthetic Nitrogen Assimilation and Associated Organic Acid Metabolism (Editors: C. H. Foyer
and G. Noctor);
(5) Clorophyll Fluorescence: A Signature of Photosynthesis (Editors: G. Papageorgiou and
Govindjee); and,
(6) Photosystem II: The Water/Plastoquinone Oxido-reductase in Photosynthesis
(Editors: T. Wydrzynski and K. Satoh).
In addition to these contracted books, on-going discussions are taking place for books on Photosys-
tem I; Functional Genomics; Protonation and ATP Synthesis; Plant Respiration; The Chlorophylls;
Photoinhibition; Global Aspects and Geochemistry; History of Photosynthesis; The Chloroplasts; C-3
and C-4 Plants; and Plant Photosynthetic Production: A Manual of Methods. Both Kluwer
([email protected]) and I ([email protected]) welcome suggestions for titles of new books (especially
in the area of respiration), for editors, for authors, and for improvement of this book series in general. In
view of the interdisciplinary character of research in photosynthesis and respiration, it is my earnest
hope that this series of books will be used in educating students and researchers not only in Plant Sci-
ences, Molecular and Cell Biology, Integrative Biology, Biotechnology, Agricultural Sciences, Micro-
biology, Biochemistry, and Biophysics, but also in Bioengineering, Chemistry, and Physics.
During the many years that I have edited this series, I have often thought of a quote by William
Safire, a columnist for the New York Times. He wrote, “To communicate, put your thoughts in order,
give them a purpose, use them to persuade, to instruct, to discover, to seduce.” Regardless of the political
ix
views of Safire, I like this quotation. I have recognized it as an important goal for writing (and editing).
It is in part because of that goal that I thank all the authors of all the books in this series –both for their
valuable writing, and for their patience when I made corrections, sometimes to their proofs!
Although Iwill continuetobeactively involved inthenewseries, Iwouldlike totakethisopportu-
nity to thank my friend John Whitmarsh for his constant support during difficult times of my life, and to
thank John, along with Colin Wraight, Don Ort, and Tony Crofts, for providing a unique intellectual
environment for my research in photosynthesis at Urbana. Others at the University of Illinois who have
collaboratedwith my laboratoryarethe late HerbertGutowsky, Enrico Gratton, and Robert Clegg. It is,
however, my graduate students and post-doctorals who did all the research and they are the ones who
were responsible for my decision to undertake the cause of education through the AIPH series. I am
highlyindebted toRajniGovindjee,myconstantcompanionsince 1957, forherlove, supportandtoler-
ance, especially of the sometimes intrusive nature of my work (such as being engrossed in e-mail when
dinner isready). Ialsofeel adeepsenseofgratitude toourchildrenSanjayGovindjee andAnitaGovindjee-
Christiansen, to their spouses Marilyn Govindjee and Morten Christiansen, and to our grandchildren
SunitaChristiansen,ArjunGovindjee, and RajivGovindjee.
August 15, 2000
Govindjee
Series Editor, Advances in Photosynthesis andRespiration
University of Illinois at Urbana-Champaign
265MorrillHall,505SouthGoodwinAvenue
Urbana, IL61801-3707,U.S.A.
Fax: [phone]
E-mail: [email protected]
URL: http://www.life.uiuc.edu/govindjee
x
Contents at a Glance
Overview
1. Photosynthesis: An Overview 1
Bacterial Photosynthesis
2. The Bacterial PhotosyntheticReaction Center: Chemical Composition and Crystal Structure 47
3. Light-Harvesting Pigment-Protein Complexes of Photosynthetic Bacteria 65
4. The Primary Electron Donor (P) ofPhotosynthetic Bacteria 87
5. The Stable Primary Electron Acceptor ofPhotosynthetic Bacteria 101
6. The Secondary Electron Acceptor ofPhotosynthetic Bacteria 111
7. The Early Electron Acceptors of Photosynthetic Bacteria Bacteriochlorophyll and Bacteriopheophytin 129
8. TheGreen Bacteria. I. The Light-Harvesting Complex, the Chlorosomes 147
9. The Green Bacteria.II. The Reaction Center Photochemistry and Electron Transport 159
10. The Secondary Electron Donor of Photosynthetic Bacteria the Cytochromes 179
Photosystem II
11. Photosystem II Introduction 199
12. The Light-Harvesting Chlorophyll-Protein Complexes ofPhotosystem II 215
13. Role ofCarotenoids in Photosynthesis 229
14. Phycobiliproteins and Phycobilisomes 251
15. The Primary Electron Donor ofPhotosystem II, P680, and Photoinhibition 271
16. The Stable Primary ElectronAcceptor andthe Secondary ElectronAcceptor 289
17. The Transient Intermediate Electron Acceptor of Photosystem II, Pheophytin 305
Oxygen Evolution
18. OxygenEvolution Introduction 323
19. OxygenEvolution The Role of Manganese 337
20. Oxygen Evolution UV Absorbance Changes associated with S-state Transitions 355
21. Oxygen Evolution Extrinsic Polypeptides and Inorganic Ionic Cofactors 365
22. The Electron Donorto EPRSpectroscopy 377
23. The Electron Donorto Optical Spectroscopy 397
24. Charge Recombination in Photosystem II andThermoluminescence 407
Photosystem I
25. Photosystem I Introduction 419
26. Photosystem-lMembrane,ComplexesandCrystals 431
27. Light-Harvesting Chlorophyll-Protein Complexes ofPhotosystem I 445
28. The Primary Electron DonorofPhotosystem I - P700 463
29. The Membrane-Bound Iron-Sulfur Proteins (FeS-A and FeS-B): Secondary Electron Acceptors of
Photosystem I 479
30. P430: The Spectral Species RepresentingtheTerminal ElectronAcceptorofPhotosystem I 505
31. The Iron-Sulfur CenterFeS-X ofPhotosystem I, the Photosystem-l Core Complex, and Interaction of
the FeS-X Domain with FeS-A/FeS-B 527
32. The Primary Electron Acceptor ofPhotosystemI 555
33. The Intermediate Electron Acceptor ofPhotosystem I – Phylloquinone (Vitamin 579
34. Mobile Electron Carriers Plastocyaninand Ferredoxin, andFerredoxin• Reductase 605
Proton Transport and Photophosphorylation
35. The Interphotosystem Complex and theRelated Complex 635
36. ProtonTranslocation andATP Synthesis 665
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