The Purple Phototrophic Bacteria Advances in Photosynthesis and Respiration
VOLUME 28
Series Editor: GOVINDJEE University of Illinois, Urbana, Illinois, U.S.A.
Consulting Editors: Julian EATON-RYE, Dunedin, New Zealand Christine H. FOYER, Newcastle upon Tyne, U.K. David B. KNAFF, Lubbock, Texas, U.S.A. Anthony L. MOORE, Brighton, U.K. Sabeeha MERCHANT, Los Angeles, California, U.S.A. Krishna NIYOGI, Berkeley, California, U.S.A. William PARSON, Seatle, Washington, U.S.A. Agepati RAGHAVENDRA, Hyderabad, India Gernot RENGER, Berlin, Germany
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 photosyn- thetic 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 crystallog- raphy 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.
For other titles published in this series, go to www.springer.com/series/5599 The Purple Phototrophic Bacteria
Edited by C. Neil Hunter University of Sheffield, United Kingdom Fevzi Daldal University of Pennsylvania, USA Marion C. Thurnauer Argonne National Laboratory, USA
and J. Thomas Beatty University of British Columbia, Canada Library of Congress Control Number: 2008932524
ISBN 978-1-4020-8814-8 (HB) ISBN 978-1-4020-8815-5 (e-book)
Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands.
www.springer.com
Cover: Four aspects of purple phototrophic bacteria, from one of their habitats through to atomic resolution structures, are superimposed on a map derived from the genome sequence of Rhodopseudomonas palustris CGA009 supplied by Professor Caroline Harwood, University of Washington, Seattle, USA.
Top left. Purple sulfur bacteria (Amoebobacter purpureus) on the shoreline of Mahoney Lake, British Columbia, Canada. Image from Professor J.T. Beatty.
Top right. Rhodobacter capsulatus streaked out on an agar plate. Image from Professor J.T. Beatty.
Bottom right. Model of a spherical chromatophore vesicle from Rhodobacter sphaeroides constructed by the in silico combination of atomic force microscopy, linear dichroism, electron microscopy, and X-ray crystallography data. Image from Dr. Melih Sener and Professor Klaus Schulten, prepared using VMD (Humphrey et al. (1996) J Mol Graphics 14: 33–38).
Bottom left. Structure of the reaction center complex from Rhodobacter sphaeroides showing the subunits and the pathway of electron transfer between cofactors. See Fig. 1, Chapter 20. Image from Professor Colin Wraight, prepared using VMD.
The camera ready text was prepared by Lawrence A. Orr, Center for Bioenergy & Photosynthesis, Arizona State University, Tempe, Arizona 85287-1604, USA.
Printed on acid-free paper
All Rights Reserved © 2009 Springer Science + Business Media B.V. 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, microfi lming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifi cally for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. This book is dedicated to Roderick K. Clayton, a pioneer of photosynthesis research From the Series Editor
Advances in Photosynthesis and Respiration Volume 28: The Purple Phototrophic Bacteria
I am delighted to announce the publication, in the • Volume 22 (2005): Photosystem II: The Light- Advances in Photosynthesis and Respiration (AIPH) Driven Water:Plastoquinone Oxidoreductase, Series, of The Purple Phototrophic Bacteria. Four edited by Thomas J. Wydrzynski and Kimiyuki distinguished authorities from three countries (UK, Satoh, from Australia and Japan. 34 Chapters, USA and Canada) have edited this Volume: C. Neil 786 pp, Hardcover. ISBN: 978-1-4020-4249-2 Hunter, the Chief Editor, Fevzi Daldal, Marion C. • Volume 21 (2005): Photoprotection, Photoin- Thurnauer and J. Thomas Beatty. This book is pro- hibition, Gene Regulation, and Environment, duced as a sequel to Volume 2 of the Series (Anoxy- edited by Barbara Demmig-Adams, William genic Photosynthetic Bacteria), published in 1995, W. III Adams and Autar K. Mattoo, from USA. and edited by Robert E. Blankenship, Michael T. 21 Chapters, 380 pp, Hardcover. ISBN: 978- Madigan and Carl E. Bauer. 14020-3564-7 • Volume 20 (2006): Discoveries in Photosynthe- sis, edited by Govindjee, J. Thomas Beatty, How- Published Volumes (2008–1994) ard Gest and John F. Allen, from USA, Canada and UK. 111 Chapters, 1304 pp, Hardcover. • Volume 27 (2008) Sulfur Metabolism in Photo- ISBN: 978-1-4020-3323-0 trophic Organisms, edited by Christiane Dahl, • Volume 19 (2004): Chlorophyll a Fluorescence: Rüdiger Hell, David Knaff and Thomas Leustek, A Signature of Photosynthesis, edited by George from Germany and USA. 24 Chapters, 551 pp, C. Papageorgiou and Govindjee, from Greece and Hardcover. ISBN: 978-4020-6862-1 USA. 31 Chapters, 820 pp, Hardcover. ISBN: • Volume 26 (2008): Biophysical Techniques 978-1-4020-3217-2 In Photosynthesis, Volume II, edited by Thijs • Volume 18 (2005): Plant Respiration: From Aartsma and Jörg Matysik, both from The Neth- Cell to Ecosystem, edited by Hans Lambers erlands. 24 Chapters, 548 pp, Hardcover. ISBN: and Miquel Ribas-Carbo, from Australia and 978-1-4020-8249-8 Spain. 13 Chapters, 250 pp, Hardcover. ISBN: • Volume 25 (2006): Chlorophylls and Bacte- 978-14020-3588-3 riochlorophylls: Biochemistry, Biophysics, • Volume 17 (2004): Plant Mitochondria: From Functions and Applications, edited by Bernhard Genome to Function, edited by David Day, A. Grimm, Robert J. Porra, Wolfhart Rüdiger, and Harvey Millar and James Whelan, from Australia. Hugo Scheer, from Germany and Australia. 37 14 Chapters, 325 pp, Hardcover. ISBN: 978-1- Chapters, 603 pp, Hardcover. ISBN: 978-1- 4020-2399-6 40204515-8 • Volume 16 (2004): Respiration in Archaea and • Volume 24 (2006): Photosystem I: The Light- Bacteria:Diversity of Prokaryotic Respiratory Driven Plastocyanin: Ferredoxin Oxidoreduc- Systems, edited by Davide Zannoni, from Italy. tase, edited by John H. Golbeck, from USA. 13 Chapters, 310 pp, Hardcover. ISBN: 978- 40 Chapters, 716 pp, Hardcover. ISBN: 978-1- 14020-2002-5 40204255-3 • Volume 15 (2004): Respiration in Archaea and • Volume 23 (2006): The Structure and Func- Bacteria: Diversity of Prokaryotic Electron tion of Plastids, edited by Robert R. Wise and Transport Carriers, edited by Davide Zannoni, J. Kenneth Wise, from USA. 27 Chapters, 575 from Italy. 13 Chapters, 350 pp, Hardcover. pp, Softcover: ISBN: 978-1-4020-6570-6, Hard- ISBN: 978-1-4020-2001-8 cover, ISBN: 978-1-4020-4060-3 • Volume 14 (2004): Photosynthesis in Algae, edited by Anthony W. Larkum, Susan Douglas and Charles F. Yocum, from USA. 34 Chapters, and John A. Raven, from Australia, Canada and 696 pp, Softcover: ISBN: 978-0-7923-3684-6. UK. 19 Chapters, 500 pp, Hardcover. ISBN: Hardcover: ISBN: 978-0-7923-3683-9 978-0-7923-6333-0 • Volume 3 (1996): Biophysical Techniques in • Volume 13 (2003): Light-Harvesting Antennas Photosynthesis, edited by JanAmesz and Arnold in Photosynthesis, edited by Beverley R. Green J. Hoff, from The Netherlands. 24 Chapters, 426 and William W. Parson, from Canada and USA. pp, Hardcover. ISBN: 978-0-7923-3642-6 17 Chapters, 544 pp, Hardcover. ISBN: 978- • Volume 2 (1995): Anoxygenic Photosynthetic 07923-6335-4 Bacteria, edited by Robert E. Blankenship, • Volume 12 (2003): Photosynthetic Nitrogen Michael T. Madigan and Carl E. Bauer, from Assimilation and Associated Carbon and USA. 62 Chapters, 1331 pp, Hardcover. ISBN: Respiratory Metabolism, edited by Christine 978-0-7923-3682-8 H. Foyer and Graham Noctor, from UK and • Volume 1 (1994): The Molecular Biology of France. 16 Chapters, 304 pp, Hardcover. ISBN: Cyanobacteria, edited by Donald R. Bryant, 978-07923-6336-1 from USA. 28 Chapters, 916 pp, Hardcover. • Volume 11 (2001): Regulation of Photosynthe- ISBN: 978-0-7923-3222-0 sis, edited by Eva-Mari Aro and Bertil Anders- son, from Finland and Sweden. 32 Chapters, 640 Further information on these books and ordering pp, Hardcover. ISBN: 978-0-7923-6332-3 instructions can be found at
viii nization; Reaction Centre Structure and Function; Loach; Chris Mackenzie; Chris Madigan; Michael Cyclic Electron Transfer Components and Energy T. Madigan; Pier Luigi Martelli; Bernd Masepohl; Coupling Reactions; Metabolic Processes; Genom- Shinji Masuda; Donna L. Mielke; Osamu Mi- ics, Regulation and Signaling; and New Applications yashita; Mamoru Nango; Robert A. Niederman; and Techniques. This book is a compilation of 48 Wolfgang Nitschke; Vladimir I. Novoderezhkin; chapters, written by leading experts who highlight Dror Noy; U. Mirian Obiozo; Melvin Okamura; the huge progress made in spectroscopic, structural Ozlem Onder; Miroslav Papiz; Pamela S. Parkes- and genetic studies of these bacteria since 1995, Loach; William W. Parson; Marcela Ávila Pérez; when the last such book was published (Anoxygenic Tomáš Polívka; Oleg G. Poluektov; Pu Qian; Jason Photosynthetic Bacteria, Volume 2 in the Advances Raymond; Bruno Robert; Brigitte R. Robinson; in Photosynthesis and Respiration Series, edited by Simona Romagnoli; Johannes Sander; Carsten Robert E. Blankenship, Michael T. Madigan and Sanders; Hugo Scheer; Simon Scheuring; Bar- Carl E. Bauer; Kluwer Academic Publishers (now bara Schoepp-Cothenet; Klaus Schulten; Melih Springer), Dordrecht). This new volume is similarly K. Şener; Aaron Setterdahl; James P. Shapleigh; intended to be the defi nitive text on these bacteria James N. Sturgis; Wesley D. Swingley; F. Robert for many years to come, and it will be a valuable Tabita; Shinichi Takaichi; Banita Tamot; Serdar resource for experienced researchers, Ph.D. students, Turkarslan; Lisa M. Utschig; Rienk van Grondelle; and advanced undergraduates in the fi elds of ecology, Michael A. van der Horst; Luuk J. van Wilderen; microbiology, biochemistry and biophysics. Scientists André Verméglio; Paulette M. Vignais; Martin interested in future applications of these bacteria J. Warren; Arieh Warshel; JoAnn C. Williams; which could harness their potential for nanotechnol- Robert D. Willows; Colin A. Wraight; Jiang Wu; ogy, solar energy research, bioremediation, or as cell Vladimir Yurkov; Davide Zannoni; and Jill Helen factories, will also fi nd the book useful. Zeilstra-Ryalls. The readers can easily fi nd the titles and the authors of the individual chapters in the Table of Content of It is a pleasure to note that the following 27 this book. Instead of repeating this information here, I participants in Volume 2 have also contributed to prefer to thank each and every author by name (listed Volume 28; they are (alphabetically): James P. Allen; in alphabetical order) that reads like a ‘Who’s Who’ Judith P. Armitage; Carl E. Bauer; J. Thomas Beatty; in the fi eld of purple phototrophic bacteria: Robert E. Blankenship; Richard J. Cogdell; Fevzi Daldal; Harry A. Frank; Caroline S. Harwood; C. Maxime T.A. Alexandre; James P. Allen; Judith Neil Hunter; J. Baz Jackson; Pierre Joliot; Gabriele P. Armitage; Herbert Axelrod; Carl E. Bauer; Klug; Robert G. Kranz; Paul A. Loach; Michael T. Christoph Benning; Edward A. Berry; Robert E. Madigan; Melvin Okamura; Pamela S. Parkes-Loach; Blankenship; Francesca Borsetti; Paula Braun; Per William W. Parson; Hugo Scheer; F. Robert Tabita; A. Bullough; Rita Casadio; Madhusudan Choud- Rienk van Grondelle; André Verméglio; Paulette hary; Toh Kee Chua; Richard J. Cogdell; Jason W. M. Vignais; Arieh Warshel; JoAnn C. Williams; and Cooley; Julius T. Csotony; Christiane Dahl; Fevzi Davide Zannoni. Daldal; Evelyne Deery; Takehisa Dewa; Timo- It is remarkable that all three editors of Volume 2 thy J. Donohue; Katie Evans; Boris A. Feniouk; (Carl E. Bauer, Robert E. Blankenship (Chief Edi- Leszek Fiedor; Anthony Fordham-Skelton; Harry tor), and Michael T. Madigan) are authors in Volume A. Frank; Elaine R. Frawley; Mads Gabrielsen; 28; and 3 of the 4 editors of Volume 28 (J. Thomas Alastair T. Gardiner; Toni Georgiou; Marie-Louise Beatty; Fevzi Daldal; and C. Neil Hunter (Chief Edi- Groot; Marilyn R. Gunner; Wolfgang Haehnel; tor)) were authors in Volume 2. Deborah K. Hanson; Caroline S. Harwood; Klaas As Volume 28 is a sequel to Volume 2, it is benefi - J. Hellingwerf; Johnny Hendriks; Theresa Hillon; cial for the readers of the new volume to consult and Jonathan Hosler; Li-Shar Huang; C. Neil Hunter; cite chapters in the earlier volume; I present below Kouji Iida; J. Baz Jackson; Pierre Joliot; Michael R. authors, titles of chapters and page numbers of all the Jones; Deborah O. Jung; Wolfgang Junge; Samuel chapters in that book. Please note that this volume Kaplan; John T. M. Kennis; Gabriele Klug; Hans was published by Kluwer Academic Publishers which Georg Koch; Jürgen Köhler; David M. Kramer; was later acquired by Springer, the publishers of the Robert G. Kranz; Alison M. Kriegel; Philip D. current volume. Laible; Jérôme Lavergne; Dong-Woo Lee; Paul A.
ix Complete List of Chapters in Anoxygenic in purple bacteria, pp 349–372 Photosynthetic Bacteria, edited by R.E. Chapter 18: H.A. Frank and R.L. Christensen Blankenship, M.T. Madigan and C.E. Bauer, (1995) Singlet energy transfer from carotenoids to Kluwer Academic Publishers, 1995 bacteriochlorophylls, pp 373–384 Chapter 19: A. Freiberg (1995) Coupling of anten- Chapter 1: J.F. Imhoff (1995) Taxonomy and nas to reaction centers, pp 385–398 physiology of phototrophic purple bacteria and green Chapter 20: R.E. Blankenship, J.M. Olson and sulfur bacteria, pp 1–15 M. Mette (1995) Antenna complexes from green Chapter 2: M.T. Madigan and J.G. Ormerod (1995) photosynthetic bacteria, pp 399–435 Taxonomy, physiology and ecology of heliobacteria, Chapter 21: P.A. Loach and P.S. Parkes-Loach pp 17–30 (1995) Structure-function relationships in core Chapter 3: B.K. Pierson and R.W. Castenholz light-harvesting complexes (LHI) as determined (1995) Taxonomy and physiology of fi lamentous by characterization of the structural subunit and by anoxygenic phototrophs, pp 31–47 reconstitution experiments, pp 437–471 Chapter 4: H. Van Gemerden and J. Mas (1995) Chapter 22: C.N. Hunter (1995) Genetic manipu- Ecology of phototrophic sulfur bacteria, pp 49–85 lation of the antenna complexes of purple bacteria, Chapter 5: R.W. Castenholz and B.K. Pierson pp 473–501 (1995) Ecology of thermophilic anoxygenic photo- Chapter 23: C.R.D. Lancaster, U. Ermler and trophs, pp 87–103 H. Michel (1995) The structures of photosynthetic Chapter 6: K. Shimada (1995) Aerobic anoxygenic reaction centers from purple bacteria as revealed by phototrophs, pp 105–122 X-ray crystallography, pp 503–526 Chapter 7: D.E. Fleischman, W.R. Evans and Chapter 24: N.W. Woodbury and J.P. Allen (1995) I.M. Miller (1995) Bacteriochlorophyll-containing The pathway, kinetics and thermodynamics of elec- rhizobium species, 123–136 tron transfer in wild type and mutant reaction centers Chapter 8: M.O. Senge and K.M. Smith (1995) of purple nonsulfur bacteria, pp 527–557 Biosynthesis and structures of the bacteriochloro- Chapter 25: W.W. Parson and A. Warshel (1995) phylls, pp 137–151 Theoretical analyses of electron-transfer reactions, Chapter 9: S.I. Beale (1995) Biosynthesis and pp 559–575 structures of porphyrins and hemes, pp 153–177 Chapter 26: M.Y. Okamura and G. Feher (1995)
Chapter 10: J.F. Imhoff and U. Bias-Imhoff (1995) Proton-coupled electron transfer reactions of QB in Lipids, quinones and fatty acids of anoxygenic pho- reaction centers from photosynthetic bacteria, pp totrophic bacteria, pp 179–205 577–594 Chapter 11: J. Weckesser, H. Mayer and G. Schulz Chapter 27: M. Volk, A. Ogrodnik and M.E. Mi- (1995) Anoxygenic phototrophic bacteria: Model chel-Beyerle (1995) The recombination dynamics of organisms for studies on cell wall macromolecules, the radical pair P+H– in external magnetic and electric pp 207–230 fi elds, pp 595–626 Chapter 12: G. Drews and J.R. Golecki (1995) Chapter 28: W. Mäntele (1995) Infrared vibrational Structure, molecular organization, and biosynthesis spectroscopy of reaction centers, pp 627–647 of membranes of purple bacteria, pp 231–257 Chapter 29: H. Scheer and G. Hartwich (1995) Chapter 13: J. Oelze and J.R. Golecki (1995) Mem- Bacterial reaction centers with modifi ed tetrapyrrole branes and chlorosomes of green bacteria: Structure, chromophores, pp 649–663 composition and development, pp 259–278 Chapter 30: U. Feiler and G. Hauska (1995) Chapter 14: A. Verméglio, P. Joliot and A. Joliot The reaction center from green sulfur bacteria, pp (1995) Organization of electron transfer components 665–685 and supercomplexes, pp 279–295 Chapter 31: J. Amesz (1995) The antenna-reaction Chapter 15: W.S. Struve (1995) Theory of elec- center complex of heliobacteria, pp 687–697 tronic energy transfer, pp 297–313 Chapter 32: R. Feick, J.A. Shiozawa and A. Ertl- Chapter 16: H. Zuber and R.J. Cogdell (1995) maier (1995) Biochemical and spectroscopic proper- Structure and organization of purple bacterial antenna ties of the reaction center of the green fi lamentous complexes, pp 315–348 bacterium, Chlorofl exus aurantiacus, pp 699–708 Chapter 17: V. Sundström and R. Van Grondelle Chapter 33: R.G. Kranz and D.L. Beckman (1995) (1995) Kinetics of excitation transfer and trapping Cytochrome biogenesis, pp 709–723
x Chapter 34: T.E. Meyer and T.J. Donohue (1995) gene cluster, pp 1083–1106 Cytochromes, iron-sulfur, and copper proteins me- Chapter 51: J.L. Gibson (1995) Genetic analysis diating electron transfer from the Cyt bc1 complex of CO2 fi xation genes, pp 1107–1124 to photosynthetic reaction center complexes, pp Chapter 52: A.J. Biel (1995) Genetic analysis and 725–745 regulation of bacteriochlorophyll biosynthesis, pp Chapter 35: K.A. Gray and F. Daldal (1995) Mu- 1125–1134 tational studies of the cytochrome bc1 complexes, Chapter 53: G.A. Armstrong (1995) Genetic pp 747–774 analysis and regulation of carotenoid biosynthesis: Chapter 36: W. Nitschke and S.M. Dracheva Structure and fuction of the crt genes and gene prod- (1995) Reaction center associated cytochromes, pp ucts, pp 1135–1157 775–805 Chapter 54: J.A. Shiozawa (1995) A foundation for Chapter 37: Z. Gromet-Elhanan (1995) The proton- the genetic analysis of green sulfur, green fi lamentous translocating F0F1 ATP synthase-ATPase complex, and heliobacteria, pp 1159–1173 pp 807–830 Chapter 55: P.M. Vignais, B. Toussaint and A. Chapter 38: J.B. Jackson (1995) Proton-translocat- Colbeau (1995) Regulation of hydrogenase gene ing transhydrogenase and NADH dehydrogenase in expression, pp 1175–1190 anoxygenic photosynthetic bacteria, pp 831–845 Chapter 56: R.G. Kranz and P.J. Cullen (1995) Reg- Chapter 39: D.C. Brune (1995) Sulfur compounds ulation of nitrogen fi xation genes, pp 1191–1208 as photosynthetic electron donors, pp 847–870 Chapter 57: J.T. Beatty (1995) Organization of Chapter 40: R. Sirevåg (1995) Carbon metabolism photosynthesis gene transcripts, pp 1209–1219 in green bacteria, pp 871–883 Chapter 58: C.E. Bauer (1995) Regulation of pho- Chapter 41: F.R. Tabita (1995) The biochemistry tosynthesis gene expression, pp 1221–1234 and metabolic regulation of carbon metabolism and Chapter 59: G. Klug (1995) Post-transcriptional
CO2 fi xation in purple bacteria, pp 885–914 control of photosynthesis gene expression, pp Chapter 42: M.T. Madigan (1995) Microbiology 1235–1244 of nitrogen fi xation by anoxygenic photosynthetic Chapter 60: R.C. Fuller (1995) Polyesters and bacteria, pp 915–928 photosynthetic bacteria: from lipid cellular inclusions Chapter 43: P.W. Ludden and G.P. Roberts (1995) to microbial thermoplastics, pp 1245–1256 The biochemistry and genetics of nitrogen fi xation Chapter 61: E.R. Goldman and D.C. Youvan by photosynthetic bacteria, pp 929–947 (1995) Imaging Spectroscopy and combinatorial Chapter 44: D. Zannoni (1995) Aerobic and mutagenesis of the reaction center and light anaerobic electron transport chains in anoxygenic harvesting II antenna, pp 1257–1268 phototrophic bacteria, pp 949–971 Chapter 62: Michiharu Kobayashi and Michihiko Chapter 45: J. Mas and H. Van Gemerden (1995) Kobayashi (1995) Waste remediation and treat- Storage products in purple and green sulfur bacteria, ment using anoxygenic phototrophic bacteria, pp pp 973–990 1269–1282 Chapter 46: J. Gibson and C.S. Harwood (1995) Degradation of aromatic compounds by nonsulfur purple bacteria, pp 991–1003 Chapter 47: J.P. Armitage, D.J. Kelly and R.E. Future AIPH and Other Related Books Sockett (1995) Flagellate motility, behavioral re- sponses and active transport in purple non-sulfur The readers of the current series are encouraged to bacteria, pp 1005–1028 watch for the publication of the forthcoming books Chapter 48: J.C. Williams and A.K.W. Taguchi (not necessarily arranged in the order of future ap- (1995) Genetic manipulation of purple photosynthetic pearance): bacteria, pp 1029–1065 • C-4 Photosynthesis and Related CO2 Concentrat- Chapter 49: M. Fonstein and R. Haselkorn (1995) ing Mechanisms (Editors:Agepati S. Raghaven- Physical mapping of Rhodobacter capsulatus: Cos- dra and Rowan Sage); mid encyclopedia and high resolution genetic map, • Photosynthesis: Perspectives on Plastid Biol- pp 1067–1081 ogy, Energy Conversion and Carbon Metabo- Chapter 50: M. Alberti, D.H. Burke and J.E. Hearst lism (Editors: Julian Eaton-Rye and Baishnab (1995) Structure and sequence of the photosynthesis Tripathy);
xi • Abiotic Stress Adaptation in Plants: Physiologi- Readers are encouraged to send their suggestions cal, Molecular and Genomic Foundation (Edi- for these and future Volumes (topics, names of future tors: Ashwani Pareek, Sudhir K. Sopory, Hans editors, and of future authors) to me by E-mail (gov@ J. Bohnert and Govindjee); illinois.edu) or fax (1-217-244-7246). • The Chloroplast: Biochemistry, Molecular Biol- In view of the interdisciplinary character of re- ogy and Bioengineering (Editors: Constantin search in photosynthesis and respiration, it is my Rebeiz, Hans Bohnert, Christoph Benning, earnest hope that this series of books will be used in Henry Daniell, Beverley R. Green, J. Kenneth educating students and researchers not only in Plant Hoober, Hartmut Lichtenthaler, Archie R. Portis Sciences, Molecular and Cell Biology, Integrative and Baishnab C. Tripathy); Biology, Biotechnology, Agricultural Sciences, Mi- • Photosynthesis In Silico: Understanding Com- crobiology, Biochemistry, and Biophysics, but also plexity from Molecules to Ecosystems (Editors: in Bioengineering, Chemistry, and Physics. Agu Laisk, Ladislav Nedbal and Govindjee); I take this opportunity to thank and congratulate and C. Neil Hunter, Fevzi Daldal, Marion Thurnauer and • Lipids in Photosynthesis: Essential and Regula- Thomas Beatty for their editorial work. My special tory Function (Editors: Hajime Wada and Norio thanks go to C. Neil Hunter, the Chief Editor of Vol- Murata). ume 28, for his painstaking work not only in editing, but also in organizing this book for Springer, and for In addition to these contracted books, the following his highly professional dealing with the typesetting topics, among others, are under consideration: process and his help in preparing this editorial. I par- ticularly thank all the 116 authors (see the list above) • Cyanobacteria of this book: without their authoritative chapters, • Genomics, Proteomics and Evolution there would be no such Volume. I give special thanks • Biohydrogen Production to Larry Orr for typesetting this book: his expertise • ATP Synthase and Proton Translocation has been crucial in bringing this book to completion. • Interactions between Photosynthesis and other We owe Jacco Flipsen, Noeline Gibson and André Metabolic Processes Tournois (of Springer) thanks for their friendly work- • Carotenoids II ing relation with us that led to the production of this • Green Bacteria and Heliobacteria book. Thanks are also due to Jeff Haas (Director of • Ecophysiology Information Technology, Life Sciences, University of • Photosynthesis, Biomass and Bioenergy Illinois at Urbana-Champaign, UIUC), Evan DeLucia • Global Aspects of Photosynthesis (Head, Department of Plant Biology, UIUC) and my • Artifi cial Photosynthesis dear wife Rajni Govindjee for constant support.
May 14, 2008 Govindjee Series Editor, Advances in Photosynthesis and Respiration University of Illinois at Urbana-Champaign, Department of Plant Biology, 265 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801-3707, USA E-mail: [email protected]; URL: http://www.life.uiuc.edu/govindjee
xii Govindjee, Series Editor
Govindjee, born in 1932, obtained his B.Sc. (Chem- included the observation of the absence of the Em- istry, Biology) and M.Sc. (Botany, Plant Physiology) erson Enhancement Effect (1960s); measurements in 1952 and 1954, from the University of Allahabad, on the lifetime of bacteriochlorophyll fl uorescence India, and his Ph.D. (Biophysics, under Eugene Rabi- (1970s); and the use of the bacterial reaction center nowitch), in 1960, from the University of Illinois at structure in homology modeling of Photosystem II, Urbana-Champaign (UIUC), IL, U.S.A. He is best particularly on its electron acceptor side (1990s). known for his research on excitation energy transfer, His current focus is on the ‘History of Photosynthe- light emission, primary photochemistry and electron sis Research,’ in ‘Photosynthesis Education’, and transfer in Photosystem II (PS II). His research, with in the ‘Possible Existence of Extraterrestrial Life.’ many collaborators, has included the discovery of a He has served on the faculty of the UIUC for ~40 short-wavelength form of chlorophyll (Chl) a func- years. Since 1999, he has been Professor Emeritus tioning in the Chl b-containing system, now called of Biochemistry, Biophysics and Plant Biology at the PS II, and of the two-light effects in Chl afl uorescence same institution. His honors include: Fellow of the and in NADP (nicotinamide adenine dinucleotide American Association of Advancement of Science; phosphate) reduction in chloroplasts (Emerson En- Distinguished Lecturer of the School of Life Sciences, hancement). Further, he has worked on the existence UIUC; Fellow and Lifetime member of the National of different spectral fl uorescing forms of Chl a and Academy of Sciences (India); President of the Ameri- the temperature dependence of excitation energy can Society for Photobiology (1980–1981); Fulbright transfer down to 4 K; basic relationships between Scholar and Fulbright Senior Lecturer; Honorary Chl a fl uorescence and photosynthetic reactions; the President of the 2004 International Photosynthesis unique role of bicarbonate on the acceptor side of PS Congress (Montréal, Canada); the 2006 Recipient II, particularly in protonation events involving the Q of the Lifetime Achievement Award from the Rebeiz B binding region; the theory of thermoluminescence Foundation for Basic Biology; and the 2007 Recipient in plants; picosecond measurements on the primary of the ‘Communication Award’ of the International photochemistry of PS II; and the use of Fluorescence Society of Photosynthesis Research (ISPR), presented Lifetime Imaging Microscopy (FLIM) of Chl a fl uo- to him at the 14th International Congress on Photo- rescence in understanding photoprotection against synthesis, held in Glasgow, Scotland, U.K. excess light. His research on photosynthetic bacteria
xiii Contents
From the Series Editor vii
Contents xv
Preface xxxi
Author Index xxxvii
Color Plates CP1–CP16
Part 1: Physiology, Ecology and Evolution
1 An Overview of Purple Bacteria: Systematics, Physiology, and Habitats 1–15 Michael T. Madigan and Deborah O. Jung Summary 2 I. Introduction 2 II. Systematics of Purple Bacteria 3 III. Physiology of Purple Bacteria 4 IV. Habitats of Purple Bacteria 7 V. Purple Bacteria in Extreme Environments 9 VI. Final Remarks 12 Acknowledgments 12 References 12
2 Evolutionary Relationships Among Purple Photosynthetic Bacteria and the Origin of Proteobacterial Photosynthetic Systems 17–29 Wesley D. Swingley, Robert E. Blankenship and Jason Raymond Summary 17 I. Introduction 18 II. The Alphaproteobacteria 18 III. Aerobic Purple Bacteria 19 IV. The Photosynthesis Gene Cluster and its Role in Evolution 20 V. Proteobacterial Comparative Genomics: Photosynthetic versus Non- Photosynthetic Proteins 21 VI. Origin and Evolution of Proteobacterial Phototrophy 22 VII. Origin and Evolution of Proteobacterial Carbon-fi xation 24 VIII. Future Directions: High-Throughput Sequencing and Metagenomics 27 Acknowledgments 28 References 28
xv 3 New Light on Aerobic Anoxygenic Phototrophs 31–55 Vladimir Yurkov and Julius T. Csotonyi Summary 31 I. Introduction 32 II. Morphological Diversity, Taxonomic Nuances, Phylogeny and Evolution 34 III. Nutritional Versatility and Peculiarities of Carbon Metabolism 40 IV. Photosynthetic Pigment Composition and Synthesis Reveal Surprises 41 V. The Mysterious Photosynthetic Apparatus of Aerobic Anoxygenic Phototrophs 44 VI. Speculation on Ecological Roles 47 VII. Concluding Remarks and Perspectives 51 Acknowledgments 52 References 52
Part 2: Molecular Structure and Biosynthesis of Pigments and Cofactors
4 Biosynthesis of Bacteriochlorophylls in Purple Bacteria 57–79 Robert D. Willows and Alison M. Kriegel Summary 57 I. Introduction 58 II. δ-Aminolevulinate to Protoporphyrin IX 59 III. Protoporphyrin IX to Bacteriochlorophyll a and b 65 IV. Concluding Remarks 75 Acknowledgments 75 References 75
5 Vitamin B12 (Cobalamin) Biosynthesis in the Purple Bacteria 81–95 Martin J. Warren and Evelyne Deery Summary 81 I. Background 81 II. Function of Cobalamin 82
III. B12 Biosynthesis in Rhodobacter capsulatus and Rhodobacter sphaeroides 83 IV. Summary of Events Required for Cobalamin Biosynthesis 84 V. Biosynthesis of Precorrin-2 and Its Onward Route Towards Siroheme and Cobalamin 86 VI. Control and Regulation of Cobalamin Biosynthesis 92 Acknowledgments 92 References 92
6 Distribution and Biosynthesis of Carotenoids 97–117 Shinichi Takaichi Summary 97 I. Introduction 98 II. Carotenogenesis 101 III. Carotenoids in Purple Bacteria 111 Acknowledgments 114 References 114
xvi 7 Membrane Lipid Biosynthesis in Purple Bacteria 119–134 Banita Tamot and Christoph Benning Summary 119 I. Introduction 120 II. Fatty Acids 122 III. Phosphoglycerolipids 123 IV. Glycoglycerolipids 126 V. Betaine Lipid 128 VI. Ornithine Lipid 129 VII. Lipid Function 130 VIII. Perspectives 131 Acknowledgments 131 References 132
Part 3: Antenna Complexes: Structure, Function and Organization
8 Peripheral Complexes of Purple Bacteria 135–153 Mads Gabrielsen, Alastair T. Gardiner and Richard J. Cogdell Summary 135 I. Introduction 136 II. Structure 136 III. The Biology of Purple Bacterial Antenna Complexes 146 IV. Final Remarks 151 Acknowledgments 151 References 151
9 Reaction Center-Light-Harvesting Core Complexes of Purple Bacteria 155–179 Per A. Bullough, Pu Qian and C. Neil Hunter Summary 155 I. Introduction 156 II. The Building Blocks: The α and β Polypeptides of Light-Harvesting Complex 1, and PufX 156 III. Circles, Arcs and Ellipses — The Light-Harvesting 1 Complex 160 IV. Monomeric Reaction Center-Light-Harvesting 1 Complexes 162 V. Monomeric Reaction Center-Light-Harvesting 1-PufX Complexes 166 VI. Dimeric Reaction Center-Light-Harvesting 1-PufX Complexes 168 VII. The Biogenesis of Core Complexes 174 Acknowledgments 175 References 175
xvii 10 Structure-Function Relationships in Bacterial Light-Harvesting Complexes Investigated by Reconstitution Techniques 181–198 Paul A. Loach and Pamela S. Parkes-Loach Summary 181 I. Introduction 182 II. Reversible Dissociation of Core Light-Harvesting 1 Complexes to a Subunit Form (B820) 182 III. Reversible Dissociation of B820 to its Fundamental Components 183 IV. Cofactor Requirements 184 V. Cofactor – Protein Interactions 184 VI. Cofactor – Cofactor Interactions 188 VII. Protein–Protein Interactions 188 VIII. Effect of PufX on Reconstitution of Light-Harvesting 1 Complexes 191 IX. In vitro versus In vivo Assembly of Complexes 192 X. Reconstitution of the Reaction Center 193 Acknowledgments 195 References 195
11 Spectroscopic Properties of Antenna Complexes from Purple Bacteria 199–212 Bruno Robert Summary 199 1. Introduction 200 II. The Different Spectral Forms of Antenna Proteins from Purple Bacteria 200 III. Antenna Proteins from Purple Bacteria: Variations Around a Structural Theme 201 IV. The Role of Ground State Interactions in Tuning the Antenna Absorption Transition 203 V. Excitonic Interactions and Disorder in Light-Harvesting Complexes 205 VI. Chromophore Interactions in Light-Harvesting Proteins: Additional Effects 207 VII. Conclusions 208 Acknowledgments 209 References 209
12 Energy Transfer from Carotenoids to Bacteriochlorophylls 213–230 Harry A. Frank and Tomáš Polívka Summary 213 I. Introduction 214 II. Carotenoid Excited States 215 III. Energy Transfer in Light-Harvesting 2 Complexes 216 IV. Energy Transfer in Light-Harvesting 1 Complexes and Reaction Centers 226 V. Outlook 227 Acknowledgments 227 References 227
xviii 13 Spectroscopy and Dynamics of Excitation Transfer and Trapping in Purple Bacteria 231–252 Rienk van Grondelle and Vladimir I. Novoderezhkin Summary 232 I. Introduction 232 II. Structure and Exciton Spectra of Light-Harvesting 1 and 2 Bacterial Antenna Complexes 235 III. Equilibration Dynamics 239 IV. Competition of Intraband B800-800 and Interband B800-850 Energy Transfer in the Light-Harvesting 2 Complex 241 V. Energy Trapping in the Core Reaction Center-Light-Harvesting 1 Complex 243 VI. Slow Conformational Motions and Excitation Dynamics in the B850-Light- Harvesting 2 Complex 244 VII. Concluding Remarks 247 Acknowledgments 248 References 248
14 Organization and Assembly of Light-Harvesting Complexes in the Purple Bacterial Membrane 253–273 James N. Sturgis and Robert A. Niederman Summary 254 I. Introduction 254 II. Themes and Variations — Structural Variability of Complexes in Native Membranes 255 III. Principles of Photosynthetic Unit Organization 257 IV. Proposals for the Functional Organization of Photosynthetic Units 263 V. In Vivo Assembly of Light-Harvesting Complexes 267 VI. Perspectives for the Next Ten Years 269 References 270
15 From Atomic-Level Structure to Supramolecular Organization in the Photosynthetic Unit of Purple Bacteria 275–294 Melih K. ùener and Klaus Schulten Summary 275 I. Introduction 276 II. Components of the Photosynthetic Unit 278 III. Quantum Physics of Light-Harvesting and Excitation Energy Transfer 279 IV. Effect of Thermal Disorder on the Spectra of Light-Harvesting Complexes 282 V. Physical Constraints Shaping the Structure of Individual Light-Harvesting Complexes 284 VI. Supramolecular Organization of the Photosynthetic Unit 286 VII. An Atomic-level Structural Model for a Photosynthetic Membrane Vesicle 287 VIII. Light-Harvesting and Excitation Transfer across a Photosynthetic Membrane Vesicle 287 IX. Conclusions 289 Acknowledgments 290 References 290
xix Part 4: Reaction Center Structure and Function
16 Structural Plasticity of Reaction Centers from Purple Bacteria 295–321 Michael R. Jones Summary 295 I. The Plastic Purple Reaction Center 296 II. Biochemical and Genetic Alteration of Polypeptide Composition 297 III. Cofactor Exclusion 299 IV. Cofactor Replacement 302 V. Helix Symmetrization 307 VI. Water and Other Unexpected Things in Electron Density Maps 310 VII. Building New Functionality 312 VIII. Conclusions 313 Acknowledgments 314 References 314
17 Structure and Function of the Cytochrome c2:Reaction Center Complex from Rhodobacter sphaeroides 323–336 Herbert Axelrod, Osamu Miyashita and Melvin Okamura Summary 323 I. Introduction 324 II. History 324
III. Structure of the Cytochrome c2:Reaction Center Complex 325 IV. Electron Transfer Reactions 327 V. Effects of Mutation 329 VI. Mechanism of Inter-Protein Electron Transfer 332 Acknowledgments 333 References 333
18 Directed Modifi cation of Reaction Centers from Purple Bacteria 337–353 JoAnn C. Williams and James P. Allen Summary 337 I. Introduction 338 II. Properties of the Cofactors 338 III. Electron Transfer Concepts 343 IV. Pathways of Electron Transfer 346 V. Conclusions 349 Acknowledgments 349 References 349
xx 19 Mechanism of Charge Separation in Purple Bacterial Reaction Centers 355–377 William W. Parson and Arieh Warshel Summary 355 I. The Reaction Sequence and Kinetics 356 II. Energies of the Radical-Pair Intermediates 357 III. Unusual Features of the Charge-Separation Reactions 360 IV. Theories of Electron-Transfer Reactions 363 Acknowledgments 370 References 370
20 The Acceptor Quinones of Purple Photosynthetic Bacteria— Structure and Spectroscopy 379–405 Colin A. Wraight and Marilyn R. Gunner Summary 379 I. Introduction 380 II. The Acceptor Quinone Reactions 382 III. Structural Features of the Acceptor Quinone Binding Sites 383 IV. Spectroscopy of the Acceptor Quinones 389
V. Functionality of the Two Quinone Positions in the QB Site 396 VI. Conclusions 398 Note Added in Proof 398 Acknowledgments 398 References 399
Part 5: Cyclic Electron Transfer Components and Energy Coupling Reactions
21 Biogenesis of c-type Cytochromes and Cytochrome Complexes 407–423 Carsten Sanders, Serdar Turkarslan, Ozlem Onder, Elaine R. Frawley, Robert G. Kranz, Hans Georg Koch and Fevzi Daldal Summary 407 I. Introduction 408 II. Maturation of c-type Cytochromes: Ccm-system I and Ccs-system II 409 III. Biogenesis of Cytochrome Complexes 415 Acknowledgments 421 References 421
xxi 22 Structural and Mutational Studies of the Cytochrome bc1 Complex 425–450 Edward A. Berry, Dong-Woo Lee, Li-Shar Huang and Fevzi Daldal Summary 425 I. Introduction 426 II. Structural and Mutational Studies 427 III. Conclusions and Perspectives 446 Acknowledgments 447 References 447
23 The Cytochrome bc1 and Related bc Complexes: The Rieske/ Cytochrome b Complex as the Functional Core of a Central Electron/Proton Transfer Complex 451–473 David M. Kramer, Wolfgang Nitschke and Jason W. Cooley Summary 452 I. Introduction 452
II. Structures of the Cytochrome bc1 and Related Rieske/Cytochrome b Complexes 453 III. Catalysis in the Rieske/Cytochrome b Complexes: The General Q-cycle Framework 455 IV. Phylogeny and Evolution 456 V. The ‘Third’ Redox Subunit is a Phylogenetic Marker 458 VI. The Rieske/Cytochrome b Complex, a Primordial Enzyme 459
VII. The Molecular Mechanism of the Qo Site: Avoiding Q-Cycle Short Circuits 460
VIII. The Quinone Reduction Site, Qi of the Cytochrome bc1 Complexes 467
IX. The Quinone Reduction Site,Qi of the Cytochrome b6 f and Related Complexes 468 X. The Functional Mechanism of the Rieske/Cytochrome b Complexes is Conserved 469 Acknowledgments 469 References 469
24 Proton Translocation and ATP Synthesis by the FoF1-ATPase of Purple Bacteria 475–493 Boris A. Feniouk and Wolfgang Junge Summary 475 I. Introduction 476 II. Structure and Rotary Catalysis 476 III. Proton Translocation and its Coupling to ATP Synthesis/Hydrolysis 478 III. Role of Proton Translocation in the Regulation of ATP Synthase 486 Acknowledgments 487 References 488
xxii 25 Proton-Translocating Transhydrogenase in Photosynthetic Bacteria 495–508 J. Baz Jackson and U. Mirian Obiozo Summary 495 I. Introduction 496 II. An Overview of the Main Structural Features of Transhydrogenase 496 III. Distribution of Transhydrogenase Among Species 496 IV. Phylogenetic Relationships between Transhydrogenases from Different Species 498 V. The Function of Transhydrogenase in Photosynthetic Bacteria 500 VI. The Mechanism of Coupling Between Hydride Transfer and Proton Translocation in Transhydrogenase 501 VII. Conformational Changes in the Coupling Reactions of Transhydrogenase 504 Acknowledgments 505 References 506
26 Functional Coupling Between Reaction Centers and Cytochrome bc1 Complexes 509–536 Jérôme Lavergne, André Verméglio and Pierre Joliot Summary 509 I. Introduction 510 II. Structure of the Protein Complexes 512 III. The Electron Donors to the Reaction Center 514 IV. Kinetics of P+ Reduction by Mobile Cytochromes 515
V. Donor Side Shuttling and Turnover of the Cytochrome bc1 Complex 517 VI. Quinone Reactions 518 VII. Supramolecular Organization in Rhodobacter sphaeroides and Rhodobacter capsulatus 519 VIII. Quinone Confi nement inRhodobacter sphaeroides 522 IX. Quinone Traffi c in the PufX– Mutant ofRhodobacter sphaeroides 522 X. The Supercomplex Model: Diffi culties and Alternative Possibilities 524 XI. Mitochondrial Supercomplexes 526
XII. Diffusion and Confi nement of Cytochromec 2: Possible Mechanisms 527 XIII. Diffusion and Confi nement of Quinones: Possible Mechanisms 528 XIV. Conclusions 529 References 530
Part 6: Metabolic Processes
27 Respiration and Respiratory Complexes 537–561 Davide Zannoni, Barbara Schoepp-Cothenet and Jonathan Hosler Summary 538 I. Aerobic Respiration 538 II. Respiration Utilizing Substrates other than Oxygen 546 III. Respiration versus Photosynthesis: Which One Came First? 553 IV. Respiration and Photosynthesis are Intermingled 553 Acknowledgments 555 References 555
xxiii 28 Carbon Dioxide Metabolism and its Regulation in Nonsulfur Purple Photosynthetic Bacteria 563–576 Simona Romagnoli and F. Robert Tabita Summary 563 I. Introduction 564 II. Regulation of cbb Gene Expression 564 Acknowledgments 575 References 575
29 Degradation of Aromatic Compounds by Purple Nonsulfur Bacteria 577–594 Caroline S. Harwood Summary 577 I. Introduction 578 II. Biochemical Themes 578 III. Species that Degrade Aromatic Compounds 579 IV. Aerobic Degradation of Aromatic Compounds by Rhodopseudomonas palustris 579 V. Anaerobic Benzoate Degradation 580 VI. The Molecular Regulation of Anaerobic Aromatic Compound Degradation 589 VII. Comparative Aspects 590 Acknowledgments 591 References 591
30 Metabolism of Inorganic Sulfur Compounds in Purple Bacteria 595–622 Johannes Sander and Christiane Dahl Summary 596 I. Introduction 596 II. Sulfur Oxidation Capabilities of Purple Bacteria 596 III. Sulfur Oxidation Pathways 602 IV. Sulfate Assimilation 612 V. Conclusions 615 Acknowledgments 616 References 616
31 Dissimilatory and Assimilatory Nitrate Reduction in the Purple Photosynthetic Bacteria 623–642 James P. Shapleigh Summary 623 I. Introduction 624 II. Denitrifi cation 624 III. Assimilation of Nitrogen 636 IV. Conclusion 638 Acknowledgments 639 References 639
xxiv 32 Swimming and Behavior in Purple Non-Sulfur Bacteria 643–654 Judith P. Armitage Summary 643 I. Introduction 644 II. Swimming 644 III. Behavioral Responses 646 Acknowledgments 653 References 653
33 Metals and Metalloids in Photosynthetic Bacteria: Interactions, Resistance and Putative Homeostasis Revealed by Genome Analysis 655–689 Francesca Borsetti, Pier Luigi Martelli, Rita Casadio and Davide Zannoni Summary 656 I. Introduction 656 II. Classifi cation of Metals and Metalloids by their Toxicity or Essentiality to Bacterial Cells (Groups I, II and III). 656 III. Metal Toxicity, Tolerance and Resistance: Generalities 657 IV. General Features on Microbial Metal Resistance/Tolerance Mechanisms 658 V. On the Bacterial Interactions with Metals and Metalloids 666 VI. Metal(loid)s Homeostasis in Phototrophs as Revealed by Genome Analysis 675 VII. Concluding Remarks 679 Acknowledgments 682 References 682
Part 7: Genomics, Regulation and Signaling
34 Purple Bacterial Genomics 691–706 Madhusudan Choudhary, Chris Mackenzie, Timothy J. Donohue and Samuel Kaplan I. Introduction 692 II. Genome Architecture and Characteristics 692 III. Gene Homologs and Metabolic Versatility 696 IV. Variation in Transcriptional Regulation and Adaptation to Changing Environments 701 V. Transposons and Genomic Rearrangements 702 VI. Circadian Clock and Gas Vesicle Proteins 702 VII. Inorganic Compounds as Reducing Power 703 VIII. Genomic Insights into the Photosynthetic Lifestyle 703 Acknowledgments 704 References 704
xxv 35 Regulation of Gene Expression in Response to Oxygen Tension 707–725 Carl E. Bauer, Aaron Setterdahl, Jiang Wu and Brigitte R. Robinson Summary 707 I. Introduction 707 II. RegB/RegA Two-Component Signal Transduction System 708 III. Aerobic repression by CrtJ 716 IV. Regulation by Fnr 721 Acknowledgments 722 References 722
36 Regulation of Genes by Light 727–741 Gabriele Klug and Shinji Masuda Summary 727 I. Introduction 728 II. Photoreceptors in Purple Photosynthetic Bacteria 728 III. Light-Dependent Responses that Do Not Depend on Photoreceptors 735 IV. Concluding Remarks 737 Acknowledgments 737 References 737
37 Regulation of Hydrogenase Gene Expression 743–757 Paulette M. Vignais Summary 743 I. Introduction 744 II. Regulation of Hydrogenase Gene Expression: Signaling and Transcription Control 744 References 755
38 Regulation of Nitrogen Fixation 759–775 Bernd Masepohl and Robert G. Kranz Summary 760 I. Nitrogen Fixation in Purple Nonsulfur Bacteria 760 II. Three Regulatory Levels of Nitrogen Fixation and Molecular Mechanisms Studied in Rhodobacter capsulatus 762 III. Other Factors that Feed into the Nitrogen Regulatory Circuitry 768 IV. Regulation in Other Purple Photosynthetic Bacteria 770 V. Future Perspectives 771 Acknowledgments 772 References 772
xxvi 39 Regulation of the Tetrapyrrole Biosynthetic Pathway 777–798 Jill Helen Zeilstra-Ryalls Summary 777 I. Introduction 778 II. Tetrapyrrole Biosynthesis Genes 778 III. Comparing and Contrasting Oxygen Control of Tetrapyrrole Biosynthesis Genes in Species of Rhodobacter 779 IV. Other Aspects of Transcriptional Regulation of Tetrapyrrole Biosynthesis Genes in Rhodobacter Species 789 V. A Genomics Perspective on the Regulation of Tetrapyrrole Biosynthesis in Other Purple Anoxygenic Photosynthetic Bacteria 789 Note Added in Proof 795 Acknowledgments 795 References 795
40 Bacteriophytochromes Control Photosynthesis in Rhodopseudomonas palustris 799–809 Katie Evans, Toni Georgiou, Theresa Hillon, Anthony Fordham-Skelton and Miroslav Papiz I. Introduction 800 II. Bacteriophytochrome Gene Organization and Regulation of Photosynthesis in Rhodopseudomonas palustris 800 III. Phytochrome Domain Organization 803 IV. Bilin Chromophore Photo-conversion 804 V. Chromophore Binding Domain of Deinococcus radiodurans Bacteriophytochrome 805 VI. Small Angle X-ray Scattering Solution Structure of Bph4 from Rhodopseudomonas palustris 805 VII. Conclusions 807 Acknowledgments 807 References 807
41 Photoreceptor Proteins from Purple Bacteria 811–837 Johnny Hendriks, Michael A. van der Horst, Toh Kee Chua, Marcela Ávila Pérez, Luuk J. van Wilderen, Maxime T.A. Alexandre, Marie-Louise Groot, John T. M. Kennis and Klaas J. Hellingwerf Summary 811 I. Introduction 812 II. Light, Oxygen, or Voltage Domains 813 III. The BLUF Domain Containing Family of Photoreceptors 816 IV. Comparison Between LOV and BLUF Domains 822 V. The Xanthopsins 823 VI. Bacteriophytochromes 827 VII. Concluding Remarks 831 Acknowledgments 832 References 832
xxvii Part 8: New Applications and Techniques
42 Foreign Gene Expression in Photosynthetic Bacteria 839–860 Philip D. Laible, Donna L. Mielke and Deborah K. Hanson Summary 840 I. Introduction 840 II. Design of a Rhodobacter-Based System for the Expression of Membrane Proteins for Structural and Functional Studies 841 III. Production of Foreign Membrane Proteins in Rhodobacter 847 IV. Optimization and Generalization of Heterologous Expression in Rhodobacter 850 V. Advantages Afforded by Rhodobacter 852 VI. Perspectives 856 Acknowledgments 856 References 856
43 Assembly of Bacterial Light-Harvesting Complexes on Solid Substrates 861–875 Kouji Iida, Takehisa Dewa and Mamoru Nango Summary 861 I. Introduction 862 II. Atomic Force Microscopy Imaging of Reassociated Bacterial Light- Harvesting Complex 1 on a Mica Substrate 864 III. Conductivity of the Bacterial Reaction Center on Chemically Modifi ed Gold Substrates Using Conductive Atomic Force Microscopy 865 IV. Molecular Assembly of Photosynthetic Antenna Core Complex on an Amino-terminated Indium Tin Oxide Electrode 869 V. Concluding Remarks 873 Acknowledgments 873 References 873
44 Optical Spectroscopy of Individual Light-Harvesting Complexes from Purple Bacteria 877–894 Jürgen Köhler Summary 877 I. Introduction 877 II. The Experimental Setup 879 III. Energy Transfer, Excitons, Strong and Weak Coupling 880 IV. Spectroscopy of Single Light-Harvesting 2 Antenna Complexes 882 V. Energy Transfer in a Single Photosynthetic Unit 889 Acknowledgements 891 References 891
xxviii 45 De novo Designed Bacteriochlorophyll-Binding Helix-Bundle Proteins 895–912 Wolfgang Haehnel, Dror Noy and Hugo Scheer Summary 895 I. Introduction 896 II. Chlorophyll Structures and Interactions with Natural Proteins 897 III. Challenges in Designing de novo Chlorophyll- and Bacteriochlorophyll- binding Proteins 899 IV. Modular Organized Chlorophyll Proteins Based on Branched Four- helix Bundle Proteins 901 V. Incorporating Chlorophylls and Bacteriochlorophylls into Self-assembling Protein Maquettes 904 VI. From Water-soluble to Amphiphilic Chlorophyll- and Bacteriochlorophyll- protein Maquettes 905 Acknowledgments 907 References 907
46 Design and Assembly of Functional Light-Harvesting Complexes 913–940 Paula Braun and Leszek Fiedor Summary 914 I. Introduction 914 II. Design of Model Light-Harvesting Proteins 916 III. Assembly of Functional Light-Harvesting 1 Complexes 924 IV. Conclusions and Prospects 935 Acknowledgments 935 References 936
47 The Supramolecular Assembly of the Photosynthetic Apparatus of Purple Bacteria Investigated by High-Resolution Atomic Force Microscopy 941–952 Simon Scheuring Summary 941 I. Introduction 942 II. Atomic Force Microscopy Analysis of the Complexes of the Bacterial Photosynthetic Apparatus 943 III. Conclusions 949 IV. Feasibilities, Limitations and Outlook 950 Acknowledgments 951 References 951
xxix 48 Protein Environments and Electron Transfer Processes Probed with High-Frequency ENDOR 953–973 Oleg G. Poluektov and Lisa M. Utschig Summary 953 I. Introduction 954 II. Low Temperature Interquinone Electron Transfer in the Photosynthetic – Reaction Center. Characterization of QB States 956 III. Electron Transfer Pathways and Protein Response to Charge Separation 963 IV. Concluding Remarks 968 Acknowledgments 969 References 969
Index 975–1013
xxx Preface
This book follows the tradition initiated in 1963, molecule approaches. New theoretical frameworks then subsequently extended in 1978 and 1995, of have had to keep pace with such technical develop- summarizing our knowledge of the photototrophic ments. Through the use of atomic force microscopy bacteria in a single volume. The fi rst book was Bac- it has been possible to examine the organization of terial Photosynthesis (Howard Gest, Anthony San clusters of individual light-harvesting and reaction Pietro and Leo P.Vernon, eds), 1963, Antioch Press, center complexes in their native membranes. We are Yellow Springs, Ohio. Fifteen years later, Roderick K. now beginning to see how the properties of native and Clayton and William R. Sistrom edited The Photosyn- modifi ed photosynthetic complexes can be harnessed thetic Bacteria (1978, Plenum Press, New York), an on the nanoscale for the design of biologically-in- indispensable book for any scientist in the fi eld at that spired energy and electron transfer devices. In addi- time. In 1995, Robert Blankenship, Michael Madigan tion to these advances, we are reminded that many and Carl Bauer edited the most complete survey of new phototrophic bacteria are still being discovered, the subject, Anoxygenic Photosynthetic Bacteria. By and although it has been 45 years since the fi rst book that time, the book had been taken under the wing on these bacteria appeared, there is much that we do of the Advances in Photosynthesis Series, initiated not know or understand. Recent publications indicate by Govindjee, as Volume 2 (Kluwer Academic Pub- that purple phototrophic bacteria are ubiquitous on lishers, Dordrecht), and now, in 2008, we come to Earth, and raise questions about their contributions to volume 28, entitled The Purple Phototrophic Bacteria global cycles of elements. Certainly, the extraordinary (Springer, Dordrecht). The word “phototrophic” is metabolic versatility of the purple bacteria, and their used because it has become clear that many purple amenability to investigation by genetic, biochemical bacteria are incapable of photosynthesis (synthesis of and biophysical techniques, will ensure that despite all cellular carbon components from CO2), although the inevitably cyclical and variable nature of science they are capable of obtaining energy in the form of funding, there will always be compelling reasons to ATP from light (using light-harvesting and reaction carry out research on the purple bacteria. center complexes that are homologous to those of Since 1995, it has become ever easier to obtain purple photosynthetic bacteria). information online, and it could be argued that the This latest survey of the fi eld is restricted to the need for a book on this topic is not as compelling purple bacteria, and does not attempt to cover, for as it might have been thirty years ago. However, example, the green sulfur bacteria. There have been there is still much value in having a hard copy of so many exciting developments since 1995 that the the diverse collection of information represented by editors felt that it was suffi ciently challenging to the 48 chapters of this book, compiled at this point summarize thirteen years of research on the purple in time and which can be held in the hand. We have bacteria. This proved to be the case, and 48 chapters attempted to impart some coherence to this project, a and more than 1000 pages were necessary to encom- process helped by using the organization of the 1995 pass the depth and breadth of the progress made in volume as a starting point. The editors have adopted studying these fascinating organisms. Since 1995, a pragmatic approach to the issue of taxonomy and, there has been an explosion of information available in the light of the ever-changing nature of specifi c from genome sequencing and related projects. The bacterial names, a rigid policy of using only the
fi rst 3-D structure of the bacterial cytochrome bc1 most recent ones has not been enforced. Thus, Rho- complex has been determined, and more structural dopseudomonas acidophila is now Rhodoblastus information has been obtained for light-harvesting acidophilus, for example, but the former name still and reaction center membrane-protein complexes. predominates in the book. Helpful lists of purple Site-directed modifi cations of light-harvesting and phototrophic bacteria, as well as lists of genes, en- reaction center complexes have been correlated with zymes, pathways, and many more attributes of these altered spectroscopic properties, even on a femtosec- bacteria, appear throughout this book. In addition, a ond timescale. Spectroscopic methods in general have section is included at the end of the present volume advanced considerably since the last volume in 1995; on new applications and techniques, with the hope an important example is the development of single that perhaps some of these will form the basis of a
xxxi fi fth book, several years from now. This new volume We are grateful to various individuals who have of- is intended to be a resource for present and future fered advice, including Govindjee, (the Series Editor), researchers in the fi elds of ecology, microbiology, John Golbeck (Editor of the book on Photosystem I, biochemistry and biophysics, some of whom might be Volume 24 in the Series), Robert Blankenship (one interested in harnessing the potential of these bacteria of the Editors of Volume 2 in the Series) and Hugo as cell factories, or for bioremediation, nanotechnol- Scheer (one of the Editors of Volume 25 that fo- ogy or solar energy research. We hope that this book cused on Chlorophylls and Bacteriochlophylls), but will help to attract a new generation of scientists to above all we thank Larry Orr, whose guidance has this fi eld. We thank the authors of all the chapters underpinned the progress of this book. Finally the for entering into the spirit of this project, which is editors thank their respective families and members intended to create a lasting work of reference, and of their laboratories for their patience throughout the a milestone in the fi eld, a staging post on a journey editing process. that still has a long way to run. May 14, 2008
C. Neil Hunter Krebs Institute for Biomolecular Research Department of Molecular Biology and Biotechnology University of Sheffi eld Firth Court, Western Bank Sheffi eld S10 2TN U.K. Email: c.n.hunter@sheffi eld.ac.uk
Fevzi Daldal Department of Biology University of Pennsylvania Philadelphia, PA 19104 U.S.A. Email: [email protected]
Marion C. Thurnauer Argonne National Laboratory Chemistry Division, E125 9700 S. Cass Avenue Argonne, Illinois 60439 U.S.A. Email: [email protected]
J. Thomas Beatty Dept. of Microbiology & Immunology University of British Columbia Rm. 4556, 2350 Health Sciences Mall Vancouver, BC, V6T 1Z3 Canada Email: [email protected]
xxxii C. Neil Hunter was born in 1954 in Yorkshire, U.K., area was hampered by a lack of molecular genetic and is a Professor in the Department of Molecular tools to study Rhodobacter sphaeroides. After return- Biology and Biotechnology at the University of ing to Bristol to learn about molecular biology in the Sheffi eld, U.K. He obtained his B.Sc. Degree at the laboratory of Professor Geoff Turner, it was possible University of Leicester in 1975, where the lectures eventually to use transposon Tn5 mutagenesis to of Professor Hans Kornberg and a laboratory project gain access to the genes encoding the enzymes for with Professor Peter Henderson inspired a lifelong bacteriochlorophyll and carotenoid biosynthesis and interest in metabolism and bioenergetics. Wanting to to develop a toolkit for site directed mutagenesis of learn about photosynthesis, Hunter moved to Bris- photosynthetic complexes. In 1984, Hunter was ap- tol University, where the laboratories of Professors pointed to a Lectureship at Imperial College, London, Trevor Griffi ths, Owen Jones and Tony Crofts were attached to the group of Professor James Barber. He studying many aspects of this topic, from pigment returned to his native Yorkshire in 1988 to a Senior biosynthesis through to electron transport. Hunter Lectureship at Sheffi eld University. In 1996 Hunter studied for his Ph.D. under the guidance of Profes- was awarded a D. Sc. by Bristol University. He is now sor Owen Jones on the topic of membrane assembly the Krebs Professor of Biochemistry at Sheffi eld, in bacterial photosynthesis, and a sabbatical visit of and continues to apply a combination of molecular Professor Robert Niederman to the Jones laboratory genetic, biochemical, structural and spectroscopic in Bristol led, in 1978, to a postdoctoral fellowship at approaches to dissect the pathways for bacteriochloro- Rutgers University, New Jersey. Hunter’s interests in phyll and carotenoid biosynthesis, and to investigate light-harvesting complexes and membrane assembly the assembly, structure, function and organization of developed further at this stage, but research in this bacterial photosynthetic membranes.
xxxiii Fevzi Daldal is a Professor in the Department of tochromes, which led him to discover the membrane
Biology, University of Pennsylvania. He obtained attached electron carrier cytochrome cy, to co-dis- his BS/MS degrees in 1974 at the Institut National cover the cytochrome cbb3 oxidase as well as novel des Sciences Appliquées (INSA) de Lyon, France, genes involved in cytochrome biogenesis. His main where he was fi rst introduced into bacterial research work on the cytochrome bc1 complex included many in François Stoeber’s group. He followed his gradu- studies, extending from the isolation of the structural ate studies on the genetics of Escherichia coli cell genes to the crystallization of the enzyme complex division at the Université Louis Pasteur, Strasbourg, to address detailed structure-function aspects using France, under the guidance of Drs. Raymond Minck molecular genetics, biochemistry and biophysical ap- (Director of the Microbiology Institute ) and Maxime proaches with Rhodobacter. Daldal’s current research Schwartz (who was at the Pasteur Institute in Paris, is centered on the structure, function, regulation, France), obtaining his doctorate in 1977. From 1969 proteomics and biogenesis of membrane cytochromes to 1977, his undergraduate and graduate studies were in Rhodobacter species. His contributions have been supported by scholarships from the French Govern- recognized by his election as a Member to the Turkish ment. In 1978, he joined, as a postdoctoral fellow, Academy of Science (2000), the American Academy Dr. Dan G. Fraenkel at Harvard Medical School, of Microbiology (2005), the American Association Microbiology and Molecular Genetics Department for the Advancement of Science (2006) and Chair of to work on E. coli intermediary metabolism and on the Gordon Conference on Molecular and Cellular the phosphofructokinase II enzyme. After joining Bioenergetics (2007). Daldal was an Editor of the the Cold Spring Harbor Laboratory as a Scientist Archives of Microbiology (2000–2006), and currently in 1983, Daldal started his studies with purple non is a member of the Editorial Board of the Journal of sulfur bacteria Rhodobacter species, focusing on cy- Bacteriology, and a reviewer for many journals.
xxxiv Marion C. Thurnauer received a B.A.(1968), colleagues demonstrated the spin correlated radical M.S.(1969),and Ph.D. (1974) in Chemistry, all from pair nature of the transient oxidized primary electron the University of Chicago, Illinois, USA. Her thesis donor and reduced quinone acceptor in photosystem I, research, under the guidance of Gerhard Closs, was in and, by comparison in purple photosynthetic bacteria. the area of photochemistry; in particular, she studied Her work (together with her colleagues) also extended magnetic interactions in radical pairs using electron to development of time-resolved magnetic resonance paramagnetic resonance (EPR) spectroscopy. In 1974, techniques, particularly for application to study pho- she became ‘hooked’ on photosynthesis research af- tochemical energy conversion. Collaborating with ter accepting a postdoctoral position at the Argonne Tijana Rajh, her research also included EPR studies of National Laboratory (ANL), Lemont, IL, USA, to photoexcited surface modifi ed nanocrystalline metal study magnetic resonance properties of excited triplet oxide colloids to mimic the energy transduction of states of chlorophylls in photosynthetic units and in natural photosynthesis. She served as Chair of the low temperature solutions. During that period, she Gordon Research Conference on Photosynthesis: and her mentors James R. Norris and Joseph J. Katz Biophysical Aspects (1994); she has organized several demonstrated that the unique electron spin polariza- symposia and workshops on magnetic resonance and tion observed in the EPR spectrum of the triplet state photosynthesis. During 2002–2003, she served on of the primary electron donor in the reaction center the Editorial Board of Biophysical Journal. In 2002, was due to radical pair induced intersystem crossing. she was awarded the 2002 Francis P. Garvan-John M. In 1977, she was promoted to staff member at ANL Olin Medal by the American Chemical Society. Other where she served as Group Leader of the Photosyn- honors include: the University of Chicago Award thesis Research Group (1993–1995) and Director of for Distinguished Performance at Argonne in 1991; the ANL Chemistry Division (1995–2003). Currently, the Agnes Fay Morgan Research Award in 1987; she is Argonne Distinguished Fellow, Emeritus. Her elected as a Fellow of the American Association for research involved studies of sequential electron the Advancement of Science in 1998. She was the transfer in natural photosynthetic systems of photo- fi rst recipient of the University of Chicago-Argonne synthetic bacteria and oxygenic photosynthesis, using Pinnacle of Education Award in 2007. primarily time-resolved EPR methods. She and her
xxxv J. Thomas Beatty is a Professor in the Department tional regulation of photosynthesis gene expression of Microbiology and Immunology at the University and elucidation of ‘superoperons’; discovery of the of British Columbia, Canada. He obtained the B.S. PufX protein and its role in quinone translocation as degree at the University of Washington in 1976, where part of the RC/LH1/PufX core complex; isolation a research project under the supervision of James and characterization of new species of phototrophic T. Staley sparked Beatty’s interest in phototrophic bacteria; mechanisms of proton translocation into the bacteria. Beatty went on to graduate studies (M.A. in RC; assembly of photosynthetic complexes; genomics 1978; Ph.D. in 1980) under the guidance of Howard and proteomics of purple bacteria. Beatty’s current Gest at Indiana University, Bloomington, IN, USA, research continues on the problems mentioned above, where he studied the metabolism of purple and green as well as on the ‘gene transfer agent’ (GTA) of Rba. bacteria. Beatty’s postdoctoral research (1980–1983), capsulatus. His contributions have been recognized in Stanley N. Cohen’s laboratory in the Department by a prize from the American Society for Microbiol- of Genetics, at the Stanford University School of ogy (2002) and a Killam Research Fellowship from Medicine, California, USA, included the discovery the Canada Council for the Arts (2008); he has been of differential degradation of light-harvesting 1 featured in popular publications such as the National (LH1) and reaction center (RC) mRNA segments Geographic and in several newspaper articles. Be- in the purple bacterium Rhodobacter capsulatus atty was an Editor of FEMS Microbiology Letters, as a process that underlies the relative amounts of and a member of the Editorial Boards of Applied LH1 and RC complexes in the cell membrane. Af- and Environmental Microbiology and the Journal ter taking up a faculty position at the University of of Bacteriology for many years. He is at present an British Columbia in 1983, Beatty has contributed to Editor of Photosynthesis Research. diverse areas of photosynthesis research: transcrip-
xxxvi Author Index
Alexandre, Maxime T. A. 811–837 Hillon, Theresa 799–809 Allen, James P. 337–353 Hosler, Jonathan 537–561 Armitage, Judith P. 643–654 Huang, Li-Shar 425–450 Axelrod, Herbert 323–336 Hunter, C. Neil 155–179
Bauer, Carl E. 707–725 Iida, Kouji 861–875 Benning, Christoph 119–134 Berry, Edward A. 425–450 Jackson, J. Baz 495–493 Blankenship, Robert E. 17–29 Joliot, Pierre 509–536 Borsetti, Francesca 655–689 Jones, Michael R. 295–321 Braun, Paula 913–940 Jung, Deborah O. 1–15 Bullough, Per A. 155–179 Junge, Wolfgang 475–493
Casadio, Rita 655–689 Kaplan, Samuel 691–706 Choudhary, Madhusudan 691–706 Kennis, John T. M. 811–837 Chua, Toh Kee 811–837 Klug, Gabriele 727–741 Cogdell, Richard J. 135–153 Koch, Hans Georg 407–423 Cooley, Jason W. 451–473 Köhler, Jürgen 877–894 Csotony, Julius T. 31–55 Kramer, David M. 451–473 Kranz, Robert G. 407–423; 759–775 Dahl, Christiane 595–622 Kriegel, Alison M. 57–79 Daldal, Fevzi 407–423; 425–450 Deery, Evelyne 81–95 Laible, Philip D. 839–860 Dewa, Takehisa 861–875 Lavergne, Jérôme 509–536 Donohue, Timothy J. 691–706 Lee, Dong-Woo 425–450 Loach, Paul A. 181–198 Evans, Katie 799–809 Mackenzie, Chris 691–706 Feniouk, Boris A. 475–493 Madigan, Michael T. 1–15 Fiedor, Leszek 913–940 Martelli, Pier Luigi 655–689 Fordham-Skelton, Anthony 799–809 Masepohl, Bernd 759–775 Frank, Harry A. 213–230 Masuda, Shinji 727–741 Frawley, Elaine R. 407–423 Mielke, Donna L. 839–860 Miyashita, Osamu 323–336 Gabrielsen, Mads 135–153 Gardiner, Alastair T. 135–153 Nango, Mamoru 861–875 Georgiou, Toni 799–809 Niederman, Robert A. 253–273 Groot, Marie-Louise 811–837 Nitschke, Wolfgang 451–473 Gunner, Marilyn R. 379–405 Novoderezhkin, Vladimir I. 231–252 Noy, Dror 895–912 Haehnel, Wolfgang 895–912 Hanson, Deborah K. 839–860 Obiozo, U. Mirian 495–493 Harwood, Caroline S. 577–594 Okamura, Melvin 323–336 Hellingwerf, Klaas J. 811–837 Onder, Ozlem 407–423 Hendriks, Johnny 811–837
xxxvii Papiz, Miroslav 799–809 Tabita, F. Robert 563–576 Parkes-Loach, Pamela S. 181–198 Takaichi, Shinichi 97–117 Parson, William W. 355–377 Tamot, Banita 119–134 Pérez, Marcela Ávila 811–837 Turkarslan, Serdar 407–423 Polívka, Tomáš 213–230 Poluektov, Oleg G. 953–973 Utschig, Lisa M. 953–973
Qian, Pu 155–179 van Grondelle, Rienk 231–252 van der Horst, Michael A. 811–837 Raymond, Jason 17–29 van Wilderen, Luuk J. 811–837 Robert, Bruno 199–212 Verméglio, André 509–536 Robinson, Brigitte R. 707–725 Vignais, Paulette M. 743–757 Romagnoli, Simona 563–576 Warren, Martin J. 81–95 Sander, Johannes 595–622 Warshel, Arieh 355–377 Sanders, Carsten 407–423 Williams, JoAnn C. 337–353 Scheer, Hugo 895–912 Willows, Robert D. 57–79 Scheuring, Simon 941–952 Wraight, Colin A. 379–405 Schoepp-Cothenet, Barbara 537–561 Wu, Jiang 707–725 Schulten, Klaus 275–294 Şener, Melih K. 275–294 Yurkov, Vladimir 31–55 Setterdahl, Aaron 707–725 Shapleigh, James P. 623–642 Zannoni, Davide 537–561; 655–689 Sturgis, James N. 253–273 Zeilstra-Ryalls, Jill Helen 777–798 Swingley, Wesley D. 17–29
xxxviii Color Plates
Fig. 1. Schematic comparison of photosynthesis gene clusters (PGC) from various purple bacteria. Lines represent transpositions of syn- tenous gene regions between two PGC. Numbers annotated above the Rhodospirillum rubrum PGC represent the location on the genome of each separate PGC segment. Genes colored in green represent BChl biosynthesis genes, orange represent carotenoid biosynthesis genes, red represent structural genes of the photosynthetic apparatus, blue represent regulatory genes and other colors represent unique genes. The black and blue lines with arrows represent inversion of the genes contained between the lines and the red lines represent shifts in position without inversions. See Chapter 2, p. 20.
C. Neil Hunter, Fevzi Daldal, Marion C. Thurnauer and J. Thomas Beatty (eds): The Purple Phototrophic Bacteria, pp. CP1–CP16. © 2009 Springer Science + Business Media B.V. Color Plates
Fig. 2. Photosynthetic and habitat diversity of aerobic anoxygenic phototrophs (AAP) A–E. In vivo absorbance spectra of cells grown under different physiological conditions, with numerals above peaks denoting LH and RC wavelengths. Insets, photographs of liquid cultures. A. Roseicyclus mahoneyensis, illuminated (dashed line) and dark (solid line). B,C. Dashed line, rich organic medium (3 g·l–1 organics); solid line, minimal acetate (1 g·l–1) medium (B. Roseococcus thiosulfatophilus, C. Erythrobacter litoralis). D. Erythromi- crobium ramosum, rich organic medium, dark (dashed line) and oligotrophic medium, light:dark regimen of 12h:12h, illuminated with diffuse ambient sunlight (solid line). E. Citromicrobium bathyomarinum strain JF1, rich organic medium (dashed line), minimal glucose medium (dotted line), compared with Erythrobacter litoralis (solid line). F. Hypothetical electron transfer system of aerobic anoxygenic photosynthesis, showing electron fl ow through major carriers: P870, special pair of BChl in RC (photoexcited state indicated by ‘*’); BChl-BPh, accessory BChl and bacteriophaeophytin in the RC; QA, quinone primary electron acceptor; Cyt bc1, cytochrome bc1 complex; Cyt c2, cytochrome c2. The symbol ‘+’ indicates that the midpoint potential of QA in all tested AAP is posi- tive and higher than in anaerobic phototrophs. G–I. Extreme environment habitats of AAP. G. Hydrothermal vent fi eld in Eastern Pacifi c Ocean, showing smoker chimney. H. Hypersaline spring system (East German Creek) in Manitoba, Canada: spring pool in foreground and playa in background, with white patches of salt precipitates. I. Cyanobacterial-Thiothrix mat development in thermal springs of Banff National Park, Alberta, Canada. See Chapter 3, p. 39.
CP2 Color Plates
Fig. 3. Representations of the β/α-protomer building blocks that comprise LH2. The β-chains are shown in blue and the α-chains in green. The BChls are shown in red and the carotenoid in pale blue. a) A view of the α/β-protomer with the pigments removed. The main BChl liganding amino acid side chains are shown. b) A view of how two adjacent β/α-protomers interact with each other, again with the pigments removed. c) Similar to b) but looking down onto the two adjacent α/β-protomers from the C-terminal side of the complex. d) The same view as a) but with the pigments included. e) A view of the α/β-protomer from Phaeospirillum (Phs.) molischianum. The main differences between d) and e) are the altered orientation of the B800 bacteriochlorin ring and the different organization of the C-terminal region of the α-apoprotein. f) A view of the α/β-protomer from Rps. acidophila strain 7050. Fig. 4. The LH2 complex from Rhodopseudomonas (Rps.) aci- Note the different amino acids shown at the C-terminal end of dophila strain 10050. a) A view looking down on the top of the the α-apoprotein that are responsible for the altered absorption complex from the presumed periplasmic surface of the membrane. properties of this B800-820 complex. The structures shown in a–d (b) A side view looking from within the presumed photosynthetic are representations of the structure of the B800-850, LH2 complex membrane with the periplasmic side of the complex uppermost. In from Rps. acidophila strain 10050. See Chapter 8, p. 138. both panels the LH2α polypeptide is green, LH2β is blue, B850 BChls are purple, B800 BChls are brown and the carotenoids are red. See Chapter 8, p. 140.
CP3 Color Plates
Fig. 5. (A) Dynamics of the transient absorption (TA) spectrum measured upon 1017 nm excitation of the LH1 of Blc. viridis at 77 K (Monshouwer et al., 1998). (B) Measured (points) and calculated (solid lines) red-shift of the TA spectrum between 0 and 400 fs upon 1017 nm excitation of the LH1 of Blc. viridis at 77K (Novoderezhkin and van Grondelle, 2002). (C) Measured (points) and modeled (solid line) TA kinetics at 1050 nm traces upon 1055 nm excitation of the LH1 of Blc. viridis at 77K (Novoderezhkin et al., 2000). See Chapter 13, p. 240.
Fig. 6. Coherent dynamics of the density matrix for a single LH2 com- plex, i.e., calculated without relaxation of populations and coherences for one realization of the disorder corresponding to a blue-shifted (top), an intermediate (middle), and a red-shifted (bottom) FL spectrum (Novoderezhkin et al., 2006). The initial population corresponds to the thermal equilibrium at room temperature (shown in the inserts by blue, green, and red for the blue-shifted, intermediate, and red-shifted spectra, respectively), initial coherences have arbitrary fi xed phases. The fi gure shows the diagonal elements of the density matrix in the site representation ρ(n,n) as a function of time. The color scale is used to indicate the absolute values of the density matrix from zero (blue) to the maximal value (red). See Chapter 13, p. 247.
CP4 Color Plates
Fig. 7. Structural models of monomeric and dimeric core complexes. In each case a side view and a space-fi lling representation is used. For the RC the complete structure is present (shown in blue), but for the LH1 (red) and helix W/PufX components (green) only the transmembrane helices are shown. a. The monomeric RC-LH1-W core complex from Rhodopseudomonas palustris (Roszak et al., 2003). b. The dimeric RC-LH1-PufX core complex of Rhodobacter (Rba.) sphaeroides. The coordinates of the LH1 αβ pairs were adopted from Roszak et al. (2003), fi tted into the tilted 3-D dimer structure from single particle analysis (Chapter 9, Bullough et al.), and adjusted according to the cryo-EM projection map in Qian et al. (2005). The transmembrane domain of PufX was taken from Tun- nicliffe et al. (2006). See Chapter 9, p. 172.
Fig. 8. Organization of the photosynthetic unit (PSU) from the supramolecular architecture to individual chlorophylls and the energy transfer network. The high-light adapted vesicle model for Rba. sphaeroides (Şener et al., 2007) is shown. The three different constitu- ent proteins and their BChls are colored as follows: LH2: green, LH1: red, RC: blue. From left to right three different rendering styles are featured. On the left, the light-harvesting proteins are shown in the tube representation (backbone only, no pigments); in the middle, the proteins are rendered transparently while the BChls are visible represented by their porphyrin rings; on the right, only the BChls are shown but this time together with their respective electronic couplings (Eq. 1). For simplicity only the strongest couplings are shown. The vesicle construction depicted here is based on atomic force microscopy data on intracytoplasmic membranes (Bahatyrova et al., 2004). Figure made with VMD (Humphrey et al., 1996). See Chapter 15, p. 288.
CP5 Color Plates
Fig. 9. Structure of the Cyt c2 : RC complex. A) Side view of the complex. The Cyt c2 is bound with heme positioned directly over the
BChl2. A small region of close contact is indicated by the circle. A conformational change, indicated by the arrow, is due to crystal packing interactions with an adjacent bound Cyt. B) View of the structure in the region between the cofactors. The heme and BChl are separated by the planar aromatic ring of Tyr (L162). The closest distance between the conjugated rings in the cofactors is 14.2 Å as shown by the long arrow. A strong tunneling pathway between the two cofactors is indicated by the short arrows. C) Open book view of the interface between the complexes. The two proteins are separated by rotating around the center line. The central region of short- range contacts (indicated by the circle) is surrounded by charged residues involved in long-range electrostatic interactions. Interacting residues are color coded. The contact between the heme (green) and the ‘hot spot’ Tyr L162 (green) is shown by the arrow. Hydrophobic residues Leu (M191), Val (M192) (black) on the RC interact with Phe (C102) on the Cyt (black). Hydrogen bonds (cyan) are formed between atoms on RC and Cyt. A cation-pi interaction is formed between Tyr (M295) and Arg (C32). Electrostatic interactions occur between negatively charged groups on the RC (red) and positively charged groups on the Cyt (violet). Other groups in van der Waals contact are shown in yellow. Modifi ed from Axelrod et al. ( 2002). See Chapter 17, p. 326.
CP6 Color Plates
Fig. 10. The cytoplasmic surface of a model LM preparation of the Rba. sphaeroides RC. (a) The LM heterodimer is shown as a solid object, with the L- and M-polypeptides shown in yellow and white, respectively, and the quinones shown as spheres with green carbons and red oxygens. The view is along the symmetry
axis, and parts of the QA quinone are visible from the outside of the complex. (b) View as in (a) but with amino acids overlaying the quinone sites shown in stick format, revealing the underlying quinones (carbons in yellow (L) or white (M), oxygens in red and nitrogens in blue). In both panels the dotted ovals show the
approximate positions of the QA and QB quinones. See Chapter 16, p. 298.
Fig. 11. Region around the HB site in the wild-type and AM149W RC complexes from Rba. sphaeroides. The protein is shown as a solid object, with the L- and M-polypeptides shown in yellow and white, respectively, and bound waters shown in cyan. The BB and QB cofactors are shown as green and beige solid objects, respectively. In (a) the HB cofactor is shown as blue sticks and the phytol chain of
PB as red sticks. In (b) the phytol chain of PB in the normal conformation is shown as red sticks and the phytol chain of PB in the alternate conformation is shown as orange sticks. See Chapter 16, p. 302.
CP7 Color Plates
Fig. 12. The reaction center (RC) complex from Rhodobacter sphaeroides comprises three subunits, a heterodimer of similar, but non-identical L (yellow) and M (blue) subunits, and subunit H (green), which caps LM on the cytosolic side of the membrane. The LM dimer binds all the cofactors, while subunit H stabilizes Fig. 13. The quinone binding sites — QA (top) and QB (bot- the structure and is involved in H+-ion uptake and transfer associ- tom) — are related by the two-fold, rotational symmetry axis of ated with electron transfer to the quinones. The L and M subunits the reaction center, which passes through the iron atom of the and all associated cofactors are arranged around a quasi-2-fold acceptor quinone complex. Both quinones are hydrogen bonded rotational symmetry axis, normal to the plane of the membrane through the carbonyl oxygens — hydrogen bonds shown in purple and passing through the primary donor (P), the special pair dimer for QA (top) and in green for QB (bottom). The binding sites of bacteriochlorophylls (BChl), and a ferrous (Fe2+) iron midway are predominantly hydrophobic, with the notable exception of between the two quinones. Electron transfer proceeds from the L212 L213 L223 Glu , Asp and Ser in the QB site, which constitute termi- excited singlet state of the primary donor (P*), via the A-branch + nal components of the H delivery pathway to QB. Note that the of cofactors — monomer BChl (B ) and BPhe (H ), bound to the A A orientations of the methoxy groups of QA and QB do not follow L subunit — to the primary quinone, QA, which is bound in a fold the two-fold rotational symmetry. (Figure prepared in VMD.) – of the M subunit. From QA the electron crosses the symmetry axis See Chapter 20, p. 385. to the secondary quinone, QB, bound in a similar fold in the L subunit. (Figure prepared in VMD.) See Chapter 20, p. 381.
CP8 Color Plates
Fig. 14. The Ccm-system I components for c-type Cyt maturation. All components of the c-type Cyt maturation, except the thiol-disulfi de oxidoreductase DsbA, are located in the cytoplasmic membrane. Both apoCyt c and heme follow different routes to the heme ligation core complex, composed of CcmI, CcmH and CcmF. Apocyt c is translocated via the Sec pathway; its cysteine thiols in the conserved CXXCH motif are fi rst oxidized by the DsbA-DsbB pathway and then reduced by the Cyt c maturation specifi c CcdA-CcmG and/or CcmH thio-reductive pathway. CcmI is involved in delivering apoCyt c to the core heme ligation complex via its different domains. Heme is translocated across the membrane, possibly via ABC–type transporter CcmABCD and is covalently attached to the conserved His residue of the heme chaperone CcmE. CcmC is involved in attaching heme to CcmE and CcmD enhances holo-CcmE production. CcmA and CcmB promote release of holo-CcmE from CcmC and CcmD. Upon formation of the thioether bonds between the apoCyt c and the heme vinyls, catalyzed by the CcmH-CcmI-CcmF complex, mature holoCyt c is released. See Chapter 21, p. 410.
Fig. 15. The Ccs-system II components for c-type Cyt maturation. Similarly to system I, all components of the system II c-type Cyt maturation pathway are located in the cytoplasmic membrane, with the exception of DsbA. The apoCyt c is translocated across the membrane by the Sec machinery and is oxidized by DsbA, then reduced by CcsX. The transmembrane proteins CcsB and CcsA form a complex that represents the system II synthetase (heme ligation core complex). The reduced apoCyt c is likely bound by the periplasmic domain of CcsB. Heme is translocated by the CcsBA complex, probably through CcsA and binds to the CcsA periplasmic WWD domain before ligation to the reduced apoCyt c. Following covalent ligation of the heme vinyl groups to the reduced cysteines of the apoCyt c CXXCH motif, the holoCyt c folds into its mature form with release from the complex. See Chapter 21, p. 412.
CP9 Color Plates
Fig. 16. Overall structure of the Rhodobacter (Rba.) capsulatus
Cyt bc1. Dimeric Cyt bc1 is depicted in the membrane, indi- cating the likely positions of the boundaries of the membrane lipid bilayer (A). The lower panels show a monomeric Cyt bc1 with the Fe/S protein ED in the b (B) or c1 (C) positions. The substrate Cyt c2 (1C2R.pdb) is modeled into its likely reactive position based on the yeast co-crystal structure (1KYO.pdb).
The regions of the Cyt bc1 structure that differ signifi cantly from the mitochondrial enzyme are colored in red, otherwise
Cyt b is shown in different shades of blue, Cyt c1 in green, Fig. 17. Stereoview of structural details of Q sites in the Rba. capsu- the Fe/S protein in yellow, and Cyt c in magenta. Hemes are α 2 latus Cyt bc1. Panel A, helices -a, A, D, and E making the Qi pocket shown in red, and the [2Fe2S] cluster is shown as a space- are colored in light pink, light pink, wine, and green, respectively. fi lled structure in yellow and orange. The Q site inhibitor o Heme bH is shown in gray and quinone bound to the Qi site in yel- stigmatellin locks the Fe/S protein ED in the b position. See low as ball-and-stick models. Panels B and C, the surface of Cyt b, Chapter 22, p. 427. showing interaction of the Fe/S protein ED with the ‘binding crater’
at the Qo site when the ED is in the ‘b’ (B) or ‘c1’ (C) positions. Cyt b is depicted using space-fi lling representation with different regions colored as described below. The white outline demarks the position of the Fe/S protein ED. Four regions surrounding the binding crater, α the cd1-cd2 helices, ef-loop, gh loop and -ef2 portion are indicated in green, magenta, yellow and cyan, respectively. At the bottom-center of the binding crater stigmatellin is shown in red. The side chains of the H135 and H156 residues of the Fe/S protein subunit are shown as ball-and-stick models. Atoms of Cyt b that are in contact (i. e., less than 3.9 Å) with the Fe/S protein ED are colored in gray, and Y302 (light green, with gray OH atom) in the α-ef helix and K329 (lime green with gray Ce and Nz atoms) between the α-ef 2 and F helices are indicated by arrows. See Chapter 22, p. 434.
CP10 Color Plates
Fig. 18. Similarities and differences in the electron transfer chains and core structures of the cyt bc1 and cyt b6 f complexes. The gross functional monomeric structures of the cyt b (blue), cyt c (red) and the ISP (yellow) coordinating portions of the cyt bc1- (left) or cyt b6 f- type (right) complexes are illustrated side-by-side as matching ribbon structures with the cofactors coordinated in each drawn as space fi lled spheres (colored as the individual subunits to which they belong). The glaring differences of the presence of an extra c-type heme
(heme ci) adjacent to the Qi (or QN) site of the cyt b6 f, as well as the presence of the non-redox active chlorophyll molecule (dark green) in this same complex, are readily seen in these side-by-side illustrations. However, in each case, a similar high (red) and low potential
(blue) chain of cofactors facilitating bifurcated electron fl ow following QH2 oxidation is easily envisioned. Both types of complex are shown with the inhibitor, stigmatellin (light green), bound at the Qo (or Qp) site as well as amino acids, pictured as stick models (blue), thought to be important for Qi (or QN) site substrate binding to aid in visually identifying the two spatially distinct Q binding sites. The illustrations have been worked up from the Rhodobacter (Rba.) capsulatus and Mastigocladus laminosus derived atomic coordinate fi les 1ZRT.pdb and 1VF5.pdb, respectively. See Chapter 23, p. 454.
CP11 Color Plates
Fig. 19. Side reactions that bypass the Q-cycle. Reactions shown are those that differ from the Q-cycle in the fate of the SQ generated at the Qo site. Details are given in the text. See Chapter 23, p. 461.
(a) (b)
Fig. 20. (a) The hydride-transfer site in 2OO5.pdb. The dI(B) component is shown in blue and dIII in green. The nucleotides are in standard atom colors (except that the C4 atoms are in yellow and are linked by the pink dashed line). H-bonds are show as green dashed lines. (b) The loop E ‘lid’ of dIII and the ‘mobile loop’ of dI closed down over the hydride transfer site of 2OO5.pdb. The nucleotides + (NADP in dIII, and the NADH analog, H2NADH, in dI) are shown in a space-fi lling format. The dI(B) polypeptide is shown in green (with its mobile loop in cyan), and the dI(A) polypeptide in yellow. The dIII polypeptide is shown in pink (with its loop E in magenta). Also shown are the RQD loop of dI and helix D/loop D of dIII (see text). See Chapter 25, p. 504.
CP12 Color Plates
Fig. 21. In response to a short fl ash of light photosynthetic reaction centers generate transmembrane voltage and release quinol (QH2); subsequent oxidation of QH2 by the cytochrome bc1 complex is coupled to proton pumping into the chromatophore lumen. The resultant ∆µ~ H+ drives protons through the ATP synthase and powers ATP synthesis. See Chapter 24 (inset from Fig 3A), page 483.
CP13 Color Plates
(i) (ii) (iii) (a) (b)
(c) (i)
(ii)
Fig. 22. Localization of cytoplasmic chemosensory proteins and loss of localization and position in PpfA mutant. (a) Rba. sphaeroides with a soluble chemoreceptor TlpC-GFP fusion and McpG-GFP, expressed from genomic replacements. (b) Fluorescence images of cells of Rba. sphaeroides expressing both (i) CheW2-YFP and (ii) CheW4-CFP from genomic replacements showing separation of the two chemotaxis pathways; (iii) overlay image. (c)(i) Cephalexin treated Rba. sphaeroides with genomically expressed TlpT-CFP showing localization at single cell distances through the fi lament. (ii) Cephalexin treated Rba. sphaeroides ∆PpfA showing loss of localization of the chemosensory clusters. The scale bars are 2 µM. See Chapter 32, p. 650.
Fig. 23. BLUF photocycle and active site structure. Panel a: active site receptor state. Panel b: active site signaling state. Panel c: typical photocycle of BLUF-domains. Panels a and b were prepared using the program PyMOL (http://www.pymol.org). Color coding for panels a and b: Grey, Carbon; Blue, Nitrogen; Red, Oxygen; Orange, Phospho- rus; Green, hydrogen bond.The structure coordinate fi le of the BLUF domain of AppA from Rba. sphaeroides (PDB ID: 1YRX) (Anderson et al., 2005) was used to create both panels. Note that for panel b the positions of the side-chain nitrogen and oxygen of Q63 were manually switched to indicate the Q-fl ip. See Chapter 41, p. 818.
CP14 Color Plates
Fig. 24. The X-ray structure of the chromophore binding domain (CBD) from Deinococcus (D.) radiodurans (Wagner et al., 2005). The PAS-2 (blue) and GAF (yellow) domains are aligned, relative to one another, by a trefoil knot formed from a loop of the GAF domain (yellow) and residues 1-35 (green) N-terminal to PAS-2. Biliverdin IXα (BV-purple) is covalently bound to Cys24 and is located in a pocket within the GAF domain formed from a β-sheet and two α-helices. See Chapter 40, p. 806.
Fig. 25. A small angle X-ray scattering (SAXS) ab-initio envelope (transparent orange) of Bph4 from Rhodopseudomonas palustris (Evans et al., 2006). The structure is a homodimer and is modelled with the crystal structures of the CBD (green) (Wagner et al., 2005) and histidine kinase (HK, cyan) (Marina et al., 2005). The positions of the BV (purple), phosphorylating histidine (red) and ATP (orange) are shown. There is no high resolution structure of a PHY domain that can be fi tted, but it is assumed to occupy the envelope between CBD and the HK domains. See Chapter 40, p. 807.
CP15 Color Plates
Fig. 26. Top:Helical net representation of shielding helices Si and binding helices Bj. The amino acids that were varied (Xk for Si and Zl for Bj) are emphasized in gray, the ligating histidine of the binding helices in green. The tables contain the amino acids of the individual helices at the varied positions. Long, solid arrows indicate the N→C direction of the peptide chains, dashed arrows the dipole moments of salt bridges. Bottom: photograph of a cellulose membrane carrying 38 modular proteins, after incubation with Ni-BPheide in buffer/
DMF and washing in buffer. Columns 2-7 correspond to identical binding helices Bj (j = 7 – 12), rows 1 - 6 to identical shielding helices
Si (i = 1 - 6). The empty spots in columns 1 and 8 correspond to modular proteins that have been punched out for mass spectrometry; the two isolated spots in the rightmost column were not used for the analyses. See Chapter 45, p. 902.
Fig. 27. Stages of LH1 formation in the presence of carotenoids in vitro. See Chapter 46, page 934.
CP16