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Genetics and Regulation of Nitrogen Fixation in Free-Living Bacteria PDF

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Genetics and Regulation of Nitrogen Fixation in Free-Living Bacteria Nitrogen Fixation: Origins, Applications, and Research Progress VOLUME 2 Genetics and Regulation of Nitrogen Fixation in Free-Living Bacteria Edited by Werner Klipp Lehrstuhl für Biologie der Mikroorganismen, Fakultät für Biologie, Ruhr-Universität Bochum, Germany Bernd Masepohl Lehrstuhl für Biologie der Mikroorganismen, Fakultät für Biologie, Ruhr-Universität Bochum, Germany John R. Gallon Biochemistry Research Group, School of Biological Sciences, University of Wales, Swansea, U.K. and William E. Newton Department of Biochemistry, Virginia Polytechnic Institute & State University, Blacksburg, U.S.A. KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW eBook ISBN: 1-4020-2179-8 Print ISBN: 1-4020-2178-X ©2005 Springer Science + Business Media, Inc. Print ©2004 Kluwer Academic Publishers Dordrecht All rights reserved No part of this eBook may be reproduced or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Springer's eBookstore at: http://ebooks.kluweronline.com and the Springer Global Website Online at: http://www.springeronline.com v TABLE OF CONTENTS Series Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix Preface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii List of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xvii Dedication – Werner Klipp and John Gallon. . . . . . . . . . . . . . . . . . . . . . . . . . . xix Chapter 1. Historical Perspective – Development of nif Genetics and Regulation in Klebsiella pneumoniae R. Dixon . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 2. The Early Years . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 3. Defining the K. pneumoniae nif Genes . . . . . . . . . . . . . . . . . . . . . . . 4 4. The Recombinant DNA Era . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5. nif Gene Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6. Coda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 Chapter 2. Genetics of Nitrogen Fixation and Related Aspects of Metabolism in Species of Azotobacter: History and Current Status C. Kennedy and P. Bishop . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27 1. Research on the Genus Azotobacter (1901-2003) . . . . . . . . . . . . . . 27 2. Application of the Tools of Genetics and Molecular Biology in Species of Azotobacter . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 3. The nif Genes encoding the Enzymes for Structure, Function, and Biosynthesis of Mo-containing Nitrogenase . . . . . . . . . . . . . 33 4. Regulation of Expression of nif and Associated Genes by Ammonium and O2 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 5. Ancillary Properties of Azotobacter Species that Aid the Efficiency of Nitrogen Fixation . . . . . . . . . . . . . . . . . . . . . . . 36 6. Discovery of Molybdenum-independent Nitrogenase Systems in A. vinelandii . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 7. Molybdenum-independent Nitrogenase systems in other Azotobacter Species . . . . . . . . . . . . . . . . . . . . . . . . . . . 44 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46 Chapter 3. Nitrogen Fixation in the Clostridia J.-S. Chen . . . . . . . . . . . . . . . . . 53 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 2. The Nitrogen-fixing Clostridia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 3. Distinctive Features of the nif Genes of the Clostridia . . . . . . . . . . . 55 vi 4. Genes for Ammonia Assimilation . . . . . . . . . . . . . . . . . . . . . . . . . . 58 5. Regulation of Nitrogen Fixation and Ammonia Assimilation . . . . . 59 6. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62 Chapter 4. Regulation of Nitrogen Fixation in Methanogenic Archaea J. A. Leigh . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 2. History and Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3. Transcriptional Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 4. Regulation of Nitrogenase Activity . . . . . . . . . . . . . . . . . . . . . . . . . 69 5. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71 Chapter 5. Nitrogen Fixation in Heterocyst-Forming Cyanobacteria T. Thiel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73 2. Structure of Heterocysts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 3. Nitrogenase Genes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78 4. Heterocyst Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81 5. Genes Important for Heterocyst Formation . . . . . . . . . . . . . . . . . . . 88 6. Heterocyst Pattern Formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95 7. Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101 Chapter 6. N2 Fixation by Non-Heterocystous Cyanobacteria J. R. Gallon . . . 111 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111 2. Non-heterocystous Cyanobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . 113 3. Patterns of N2 Fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133 Chapter 7. Nitrogen Fixation in the Photosynthetic Purple Bacterium Rhodobacter capsulatus B. Masepohl, T. Drepper and W. Klipp . . . . . . . . . . . 141 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141 2. Organization of Nitrogen-fixing Genes . . . . . . . . . . . . . . . . . . . . . . 142 3. The Nitrogen-fixation Regulon of R. capsulatus . . . . . . . . . . . . . . . 155 4. Ammonium Control of Synthesis and Activity of both Nitrogenases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158 5. Environmental Factors Controlling Nitrogen Fixation . . . . . . . . . . 161 6. Linkage of Nitrogen Fixation, Photosynthesis, and Carbon Dioxide Assimilation . . . . . . . . . . . . . . . . . . . . . . . . 162 7. Nitrogen Fixation in other Photosynthetic Purple Bacteria . . . . . . . 163 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 vii Chapter 8. Post-translational Regulation of Nitrogenase in Photosynthetic Bacteria S. Nordlund and P. W. Ludden . . . . . . . . . . . . . . . . . . 175 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175 2. Discovery of Nitrogen Fixation by Photosynthetic Bacteria . . . . . . 176 3. In vitro Studies of Nitrogenase in Photosynthetic Bacteria . . . . . . . 177 4. The Protein Era . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 5. Evidence for the Drat/Drag System in other Organisms . . . . . . . . . 182 6. Other ADP-Ribosylations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 7. Genetics of the Drag/Drat System . . . . . . . . . . . . . . . . . . . . . . . . . . 185 8. Signal Transduction to Drat and Drat . . . . . . . . . . . . . . . . . . . . . . . 185 9. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190 Chapter 9. Regulation of Nitrogen Fixation in Free-Living Diazotrophs M. J. Merrick . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 2. General Nitrogen Control Systems . . . . . . . . . . . . . . . . . . . . . . . . . 198 3. nif-specific Nitrogen Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204 4. Nitrogen Control of Nitrogenase Activity . . . . . . . . . . . . . . . . . . . . 211 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 214 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 Chapter 10. Molybdenum Uptake and Homeostasis R. N. Pau . . . . . . . . . . . . 225 1. Molybdenum Outside Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225 2. Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230 3. Cytoplasmic Molybdate-binding Proteins . . . . . . . . . . . . . . . . . . . . 236 4. The ATP-binding Protein of the Molybdate Transporter . . . . . . . . 242 5. The Regulatory Protein, ModE . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251 Chapter 11. Electron Transport to Nitrogenase: Diverse Routes for a Common Destination K. Saeki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 2. Direct Electron Donors to the Fe Protein of Nitrogenase . . . . . . . . 259 3. Reduction of Electron-donor Proteins for the Fe Protein . . . . . . . . 269 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281 Chapter 12. Prospects J. R. Gallon and B. Masepohl . . . . . . . . . . . . . . . . . . . . 291 Subject Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297 This page intentionally left blank ix SERIES PREFACE Nitrogen Fixation: Origins, Applications, and Research Progress Nitrogen fixation, along with photosynthesis as the energy supplier, is the basis of all life on Earth (and maybe elsewhere too!). Nitrogen fixation provides the basic component, fixed nitrogen as ammonia, of two major groups of macromolecules, namely nucleic acids and proteins. Fixed nitrogen is required for the N-containing heterocycles (or bases) that constitute the essential coding entities of deoxyribonucleic acids (DNA) and ribonucleic acids (RNA), which are responsible for the high-fidelity storage and transfer of genetic information, respectively. It is also required for the amino-acid residues of the proteins, which are encoded by the DNA and that actually do the work in living cells. At the turn of the millennium, it seemed to me that now was as good a time as any (and maybe better than most) to look back, particularly over the last 100 years or so, and ponder just what had been achieved. What is the state of our knowledge of nitrogen fixation, both biological and abiological? How has this knowledge been used and what are its impacts on humanity? In an attempt to answer these questions and to capture the essence of our current knowledge, I devised a seven-volume series, which was designed to cover all aspects of nitrogen-fixation research. I then approached my long-time contact at Kluwer Academic Publishers, Ad Plaizier, with the idea. I had worked with Ad for many years on the publication of the Proceedings of most of the International Congresses on Nitrogen Fixation. My personal belief is that congresses, symposia, and workshops must not be closed shops and that those of us unable to attend should have access to the material presented. My solution is to capture the material in print in the form of proceedings. So it was quite natural for me to turn to the printed word for this detailed review of nitrogen fixation. Ad’s immediate affirmation of the project encouraged me to share my initial design with many of my current co-editors and, with their assistance, to develop the detailed contents of each of the seven volumes and to enlist prospective authors for each chapter. There are many ways in which the subject matter could be divided. Our decision was to break it down as follows: nitrogenases, commercial processes, and relevant chemical models; genetics and regulation; genomes and genomics; associative, endophytic, and cyanobacterial systems; actinorhizal associations; leguminous symbioses; and agriculture, forestry, ecology, and the environment. I feel very fortunate to have been able to recruit some outstanding researchers as co- editors for this project. My co-editors were Mike Dilworth, Claudine Elmerich, John Gallon, Euan James, Werner Klipp, Bernd Masepohl, Rafael Palacios, Katharina Pawlowski, Ray Richards, Barry Smith, Janet Sprent, and Dietrich Werner. They worked very hard and ably and were most willing to keep the volumes moving along reasonably close to our initial timetable. All have been a pleasure to work with and I thank them all for their support and unflagging interest.

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