Biochemistry of Nickel

BIOCHEMISTRY OF THE ELEMENTS

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Biochemistry of Nickel

Robert P. Hausinger Departments of Microbiology and Biochemistry Michigan State University East Lansing, Michigan

SPRINGER SCIENCE+BUSINESS MEDIA, LLC

Library of Congress Catalog1ng-1n-Publ1cat1on Data

Hausinger, Robert P. Biochemistry of n1ckel 1 Robert P. Hausinger.

p. cm. -- <B1ochemistry of the elements v. 12J Includes b1bllograph1cal references and index. ISBN 978-1-4757-9437-3 ISBN 978-1-4757-9435-9 (eBook) DOI 10.1007/978-1-4757-9435-9 1. N1ckel--Metabol1sm. 2. Nickel enzymes. 3. Nlckel--Toxicology.

4. N1ckel 1n the body. I. Title. II. Ser1es. [ONLM: 1. Nickel--metabol ism. 2. Biochemistry. au 130 66144

1980 V, 12 1980) OP535.N6H38 1993 574.19"214--dc20 DNLM/DLC for Library of Congress

ISBN 978-1-4757-9437-3

© 1993 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1993 Softcover reprint of the hardcover 1 st edition 1993

Ali rights reserved

93-21371 CIP

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

To Sue, Michael, and Melanie

Preface

This book represents an attempt to summarize the rapidly growing body of knowledge concerning the biochemistry of nickel. This metal ion is typically considered in terms of its harmful effects on biological systems. For example, numerous toxic effects of nickel salts on microbes, plants, and animals have been described, and the carcinogenic properties of nickel compounds in an­imals have recently been extensively studied. Nevertheless, it is now clear that nickel is essential for several metabolic processes, and four types of nickel­containing enzymes have been identified. Many microorganisms, plants, and animals possess mechanisms to transport this metal ion and incorporate it into specific proteins or organic complexes. As an extreme example, the plant Sebertia acuminata accumulates nickel ion as a complex with an organic acid to a concentration of 25% (dry weight) in its sap. Here, I attempt to provide a balanced discussion of nickel biochemistry that includes descriptions of both its harmful and its beneficial effects in microorganisms, plants, and an­imals.

This book divides the multiple facets of nickel biochemistry into nine chapters. Chapter 1 serves as a general introduction to the harmful and ben­eficial aspects of nickel from a historical perspective. In addition, it provides a summary of nickel concentrations, distributions, and fluxes in the environ­ment. The coordination chemistry and spectroscopic properties of nickel are briefly summarized in Chapter 2. Chapters 3 through 6 describe the four distinct types of nickel-containing enzymes: urease, hydrogenase, carbon monoxide dehydrogenase, and methyl coenzyme M reductase. The properties of the nickel-dependent proteins and their nickel metallocenters are discussed in detail, along with related genetic information. Furthermore, the evidence for and properties of elaborate biosynthetic systems that function to specifically incorporate this metal ion into certain of these proteins are described. Chapter 7 focuses on other aspects of microbial nickel metabolism, including the mechanisms of nickel transport, toxicity, and resistance. The interactions between plants and nickel are described in Chapter 8. Topics discussed in this chapter include the evidence that nickel is necessary to plant life, the mechanisms of toxicity and resistance, and the special case of the nickel-

vii

viii Preface

hyperaccumulating plants. Finally, Chapter 9 describes animal nickel metab­olism. The mechanisms for nickel uptake, transport, and elimination are de­scribed, the evidence for a nickel requirement in animals is evaluated, and the toxic and carcinogenic effects of nickel are summarized.

When Dr. Earl Frieden asked whether I would be willing to undertake writing a book on the biochemistry of nickel, I realized that no one person can be expert in all aspects of this field. Additionally, it was clear to me that any book on this topic would age rapidly because of the brisk pace of research in this area. Nevertheless, I felt that a critical and detailed summary of our current understanding of the biological interactions of this metal ion would be timely and of widespread interest. Furthermore, such a book would allow one to point out the key unanswered questions remaining in this field and perhaps help to define future research directions involving the biochemistry of nickel. I accepted his offer to write this book and have strived to present an up-to-date synopsis of this field. I hope that the reader will enjoy learning about this fascinating biological metal and be stimulated to pursue research in the challenging area of nickel biochemistry.

Robert P. Hausinger

Contents

1. Introduction

1.1 Historical Perspectives on Nickel . . . . . . . . . . . . . . . . . . . . . . . I 1.2 Environmental Aspects of Nickel . . . . . . . . . . . . . . . . . . . . . . 5 I. 3 Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I 0

2. Chemistry of Nickel

2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 2.2 Coordination Chemistry of Nickel . . . . . . . . . . . . . . . . . . . . 14

2.2.1 High Oxidation States of Nickel: Ni(IV, III) . . . . . . . . . 15 2.2.2 Nickei(II) Coordination Chemistry . . . . . . . . . . . . . . . 15 2.2.3 Low Oxidation States of Nickel: Ni(I, 0, -I) . . . 17

2.3 Spectroscopic Properties of Nickel . . . . . . . . . . . . . . . 17 2.3.1 Electronic Spectroscopy of Nickel Compounds . . . . . . . 17 2.3.2 Magnetic Properties of Nickel Compounds . . . . . . . . . . 19

2.4 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

3. Urease

3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . 23 3.2 General Properties of Nickel-Containing Ureases . . . . 25 3.3 Characteristics ofthe Urease Nickel Active Site . . . . . . 30

3.3.1 Crystallographic Analysis of Urease . . . . . . . . . . . . . . . 31 3.3.2 Inhibition Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 3.3.3 Biophysical and Spectroscopic Analysis of the Urease

Active Site . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 3.3.4 Chemical Modification Studies ofthe Urease Active Site 35

ix

X Contents

3.3.5 Site-Directed Mutagenesis of the Urease Active Site . . . 37 3.3.6 Structure ofthe Urease Active Site and the

Mechanism of Catalysis . . . . . . . . . . . . . . . . . . . . . . . . . 39 3.4 Chemical Models of Urease . . . . . . . . . . . . . . . . . . . . . . . . . . . 41 3.5 Mechanism ofUrease Metallocenter Assembly . . . . . . . . . . . . 43

3.5.1 Urease Metallocenter Stability . . . . . . . . . . . . . . . . . . . . 44 3.5.2 Reconstitution of Urease Apoenzyme . . . . . . . . . . . . . . 45 3.5.3 Accessory Genes Facilitating Nickel Incorporation

into Bacterial Urease . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46 3.5.4 Accessory Genes for Urease Activation in Eucaryotes 48

3.6 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50

4. Hydrogenase

4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 4.2 Evidence for Nickel in Hydrogenases . . . . . . . . . . . . . . . . . . . . 60 4.3 General Properties of Nickel-Containing Hydrogenases . . . . . 61 4.4 Characterization of the Hydrogenase Nickel Center . . . . . . . . 69

4.4.1 Inactive and Active Forms of Hydrogenase . . . . . . . . . . 70 4.4.2 EPR Spectroscopy of Hydrogenases . . . . . . . . . . . . . . . . 70 4.4.3 Other Spectroscopic Studies of Hydrogenases . . . . . . . . 74 4.4.4 Comparison to Nickel Model Compounds . . . . . . . . . . 77

4.5 Hydrogenase Structure: Characterization of Nickel Ligands . . 81 4.6 Biosynthesis of the Hydrogenase Nickel Center . . . . . . . . . . . 85

4.6.1 Hydrogenase Accessory Genes in E. coli . . . . . . . . . . . . 86 4.6.2 Hydrogenase Accessory Genes in Other Microorganisms 88

4. 7 Nickel-Dependent Transcriptional Regulation of Hydrogenase 91 4.8 Perspective .......... ·

0 • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • 92

References ............................ 0 • • • • • • • • • • • • 92

5. Carbon Monoxide Dehydrogenase

5.1 Introduction .. 0 • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • 107 5.2 CO Dehydrogenases Involved in Autotrophic Growth . . . . . . 107

5.2.1 Acetogen CO Dehydrogenases Are Nickel-Containing Enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I 08

5.2.2 Acetogen CO Dehydrogenases Function as Acetyl Coenzyme A Synthases . . . . . . . . . . . . . . . . . . . . . . . . . . II 0

Contents xi

5.2.3 Molecular Biological Studies of Acetogen Acetyl Coenzyme A Synthase . . . . . . . . . . . . . . . . . . . . . . . . . . 114

5.2.4 Properties of the Acetogen Acetyl Coenzyme A Synthase Nickel Active Site . . . . . . . . . . . . . . . . . . . . . . 115

5.2.5 Chemical Modeling of Acetogen Acetyl Coenzyme A Synthase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120

5.2.6 CO Dehydrogenase-Dependent Autotrophic Growth in Nonacetogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

5.3 CO Dehydrogenases Involved in Aceticlastic Methanogenesis 124 5.3.1 General Properties of Aceticlastic Methanogen CO

Dehydrogenase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 5.3.2 CO Dehydrogenase Functions in Aceticlastic

Methanogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126 5.3.3 Molecular Biological Studies of Aceticlastic

Methanogen CO Dehydrogenase . . . . . . . . . . . . . . . . . . 129 5.3.4 Properties of the Aceticlastic Methanogen CO

Dehydrogenase Nickel Active Site . . . . . . . . . . . . . . . . . 130 5.4 CO Dehydrogenases Not Involved in Acetate Metabolism . . . 132

5.4.1 Rhodospirillum rubrum CO Dehydrogenase . . . . . . . . . 132 5.4.2 Other CO Dehydrogenases . . . . . . . . . . . . . . . . . . . . . . . 136

5.5 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

6. Methyl Coenzyme M Reductase

6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 6.2 Evidence for Nickel in Methyl Coenzyme M Reductase . . . . . 149 6.3 Structure of Coenzyme F430 . . . . . . . . . . . . . . . . . . . . . . . . . . . 150 6.4 General Properties of Methyl Coenzyme M Reductase . . . . . 153

6.4.1 Protein Characterization . . . . . . . . . . . . . . . . . . . . . . . . . 153 6.4.2 Coenzyme Binding Properties . . . . . . . . . . . . . . . . . . . . 156 6.4.3 Protein Sequence Analysis . . . . . . . . . . . . . . . . . . . . . . . 157 6.4.4 Enzymology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158

6.5 Characterization of the Nickel Center . . . . . . . . . . . . . . . . . . . 161 6.5.1 Nonplanarity ofthe Corphin Ring . . . . . . . . . . . . . . . . . 161 6.5.2 Coenzyme F430 Axial Ligation . . . . . . . . . . . . . . . . . . . . 162 6.5.3 Redox Activity of F430 . . . . . . . . . . . . . . . . . . . . . . . . . . 165 6.5.4 Mechanism of Catalysis . . . . . . . . . . . . . . . . . . . . . . . . . 169

6.6 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 7 3

xii Contents

7. Microbial Nickel Metabolism

7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181 7.2 Microbial Nickel Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . 181

7 .2.1 Nickel Transport into Enteric Bacteria . . . . . . . . . . . . . 182 7 .2.2 Nickel Transport into Alcaligenes eutrophus . . . . . . . . . 185 7 .2.3 Nickel Transport into Other Microorganisms . . . . . . . . 186

7.3 Nickel Toxicity and Resistance Mechanisms in Microorganisms 188 7 .3.1 Mechanisms of Nickel Toxicity in Microorganisms . . . 188 7.3.2 Environmental Influences on Nickel Toxicity . . . . . . . . 189 7 .3.3 Mechanisms of Nickel Resistance in Microorganisms 191

7.4 Other Aspects of Microbial Nickel Metabolism . . . . . . . . . . . 195 7.5 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198

8. Plant Nickel Metabolism

8.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203 8.2 Nickel Functions and Requirements in Plants . . . . . . . . . . . . 203 8.3 Nickel Transport in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

8.3.1 Uptake ofNickel from the Environment . . . . . . . . . . . . 205 8.3.2 Systemic Transport ofNickel . . . . . . . . . . . . . . . . . . . . . 206

8.4 Nickel Toxicity and Resistance in Plants . . . . . . . . . . . . . . . . . 208 8.5 Hyperaccumulators of Nickel . . . . . . . . . . . . . . . . . . . . . . . . . . 209

8.5.1 Distribution of Nickel Hyperaccumulators . . . . . . . . . . 210 8.5.2 Biochemistry of Nickel Metabolism in

Hyperaccumulators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 212 8.5.3 Functional Advantage ofNickel Hyperaccumulation . . 216

8.6 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 7

9. Animal Nickel Metabolism

9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221 9.2 Flux of Nickel in Animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221

9.2.1 Uptake ofNickel from the Environment . . . . . . . . . . . . 222 9.2.2 Systemic Transport of Nickel . . . . . . . . . . . . . . . . . . . . . 224 9.2.3 Tissue Distribution of Nickel . . . . . . . . . . . . . . . . . . . . . 227 9.2.4 Elimination ofNickel . . . . . . . . . . . . . . . . . . . . . . . . . . . 229 9.2.5 Cellular Internalization of Nickel . . . . . . . . . . . . . . . . . . 231

Contents xiii

9.3 Essentiality and Functional Roles of Nickel in Animals 233 9.3.1 Evidence That Nickel Is Required in Chickens . . . . . . . 233 9.3.2 Evidence That Nickel Is Required in Monogastric

Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234 9.3.3 Evidence That Nickel Is Required in Ruminants . . . . . 236 9.3.4 Evidence That Nickel Is Required in Invertebrates . . . . 237 9.3.5 Possible Roles for Nickel in Animals . . . . . . . . . . . . . . . 237

9.4 Harmful Effects of Nickel in Animals . . . . . . . . . . . . . . . . . . . 240 9 .4.1 Immunological Effects of Nickel . . . . . . . . . . . . . . . . . . 241 9.4.2 General Toxicity of Nickel . . . . . . . . . . . . . . . . . . . . . . . 243 9.4.3 Embryotoxicity of Nickel . . . . . . . . . . . . . . . . . . . . . . . . 246 9.4.4 Carcinogenicity ofNickel . . . . . . . . . . . . . . . . . . . . . . . . 247 9.4.5 Tissue Culture Studies Related to Nickel Carcinogenesis 250 9.4.6 Mechanisms of Nickel Damage . . . . . . . . . . . . . . . . . . . 253

9.5 Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271