SPIN STATES IN BIOCHEMISTRY AND INORGANIC CHEMISTRYINFLUENCE ON STRUCTURE AND REACTIVITY

EDITORS MARCEL SWART • MIQUEL COSTAS

Spin States in Biochemistryand Inorganic Chemistry

Spin States in Biochemistryand Inorganic Chemistry

Influence on Structure and Reactivity

Edited by

MARCEL SWARTInstitut de Quımica Computacional i Catalisi & Departament de Quımica, Universitat de Girona, Spain

andInstitucio Catalana de Recerca i Estudis Avancats (ICREA), Barcelona, Spain

MIQUEL COSTASInstitut de Quımica Computacional i Catalisi & Departament de Quımica, Universitat de Girona, Spain

This edition first published 2016© 2016 John Wiley & Sons, Ltd

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Library of Congress Cataloging-in-Publication Data

Spin states in biochemistry and inorganic chemistry : influence on structure and reactivity / edited by Marcel Swart and Miquel Costas.pages cm

Includes bibliographical references and index.ISBN 978-1-118-89831-4 (cloth)

1. Nuclear spin. 2. Free radicals (Chemistry) 3. Biochemistry. 4. Chemistry, Inorganic. I. Swart, Marcel, 1971– editor. II. Costas Salgueiro,Miquel, editor.

QP527.S65 2016612′.01524–dc23

2015019422

A catalogue record for this book is available from the British Library.

ISBN: 9781118898314

Cover Image supplied by Marcel Swart.

Set in 10/12pt Times by Aptara Inc., New Delhi, India.

1 2016

Voor Elvira en PoppyPer la Judit, la Mireia i l’Ariadna

Contents

About the Editors xv

List of Contributors xvii

Foreword xxi

Acknowledgments xxiii

1 General Introduction to Spin States 1Marcel Swart and Miquel Costas1.1 Introduction 11.2 Experimental Chemistry: Reactivity, Synthesis and Spectroscopy 21.3 Computational Chemistry: Quantum Chemistry and Basis Sets 4

References 4

2 Application of Density Functional and Density Functional Based Ligand Field Theoryto Spin States 7Claude Daul, Matija Zlatar, Maja Gruden-Pavlovic and Marcel Swart2.1 Introduction 72.2 What Is the Problem with Theory? 9

2.2.1 Density Functional Theory 92.2.2 LF Theory: Bridging the Gap Between Experimental and Computational

Coordination Chemistry 112.3 Validation and Application Studies 15

2.3.1 Use of OPBE, SSB-D and S12g Density Functionals for Spin-State Splittings 172.3.2 Application of LF-DFT 21

2.4 Concluding Remarks 25Acknowledgments 26References 27

3 Ab Initio Wavefunction Approaches to Spin States 35Carmen Sousa and Coen de Graaf3.1 Introduction and Scope 353.2 Wavefunction-Based Methods for Spin States 35

3.2.1 Single Reference Methods 363.2.2 Multireference Methods 373.2.3 MR Perturbation Theory 393.2.4 Variational Approaches 403.2.5 Density Matrix Renormalization Group Theory 40

3.3 Spin Crossover 413.3.1 Choice of Active Space and Basis Set 41

viii Contents

3.3.2 The HS–LS Energy Difference 433.3.3 Light-Induced Excited Spin State Trapping (LIESST) 453.3.4 Spin Crossover in Other Metals 47

3.4 Magnetic Coupling 473.5 Spin States in Biochemical and Biomimetic Systems 503.6 Two-State Reactivity 523.7 Concluding Remarks 52

References 53

4 Experimental Techniques for Determining Spin States 59Carole Duboc and Marcello Gennari4.1 Introduction 594.2 Magnetic Measurements 61

4.2.1 g-Anisotropy and Zero-Field Splitting (zfs) 644.2.2 Unquenched Orbital Moment in the Ground State 644.2.3 Exchange Interactions 644.2.4 Spin Transitions and Spin Crossover 66

4.3 EPR Spectroscopy 664.4 Mossbauer Spectroscopy 704.5 X-ray Spectroscopic Techniques 744.6 NMR Spectroscopy 774.7 Other Techniques 804.A Appendix 81

4.A.1 Theoretical Background 814.A.2 List of Symbols 82References 82

5 Molecular Discovery in Spin Crossover 85Robert J. Deeth5.1 Introduction 855.2 Theoretical Background 85

5.2.1 Spin Transition Curves 885.2.2 Light-Induced Excited Spin State Trapping 89

5.3 Thermal SCO Systems: Fe(II) 905.4 SCO in Non-d6 Systems 935.5 Computational Methods 955.6 Outlook 98

References 99

6 Multiple Spin-State Scenarios in Organometallic Reactivity 103Wojciech I. Dzik, Wesley Bohmer and Bas de Bruin6.1 Introduction 1036.2 “Spin-Forbidden” Reactions and Two-State Reactivity 1046.3 Spin-State Changes in Transition Metal Complexes 107

6.3.1 Influence of the Spin State on the Kinetics of Ligand Exchange 1086.3.2 Stoichiometric Bond Making and Breaking Reactions 1096.3.3 Spin-State Situations Involving Redox-Active Ligands 115

Contents ix

6.4 Spin-State Changes in Catalysis 1196.4.1 Catalytic (Cyclo)oligomerizations 1196.4.2 Phillips Cr(II)/SiO2 Catalyst 1216.4.3 SNS–CrCl3 Catalyst 123

6.5 Concluding Remarks 125References 126

7 Principles and Prospects of Spin-States Reactivity in Chemistry and BioinorganicChemistry 131Dandamudi Usharani, Binju Wang, Dina A. Sharon and Sason Shaik7.1 Introduction 1317.2 Spin-States Reactivity 132

7.2.1 Two-State and Multi-State Reactivity 1337.2.2 Origins of Spin-Selective Reactivity: Exchange-Enhanced Reactivity and Orbital

Selection Rules 1377.2.3 Considerations of Exchange-Enhanced Reactivity versus Orbital-Controlled

Reactivity 1407.2.4 Consideration of Spin-State Selectivity in H-Abstraction: The Power of EER 1427.2.5 The Origins of Mechanistic Selection – Why Are C–H Hydroxylations Stepwise

Processes? 1467.3 Prospects of Two-State Reactivity and Multi-State Reactivity 148

7.3.1 Probing Spin-State Reactivity 1487.3.2 Are Spin Inversion Probabilities Useful for Analyzing TSR? 150

7.4 Concluding Remarks 151References 151

8 Multiple Spin-State Scenarios in Gas-Phase Reactions 157Jana Roithova8.1 Introduction 1578.2 Experimental Methods for the Investigation of Metal-Ion Reactions 1588.3 Multiple State Reactivity: Reactions of Metal Cations with Methane 1608.4 Effect of the Oxidation State: Reactions of Metal Hydride Cations with Methane 1638.5 Two-State Reactivity: Reactions of Metal Oxide Cations 1648.6 Effect of Ligands 1718.7 Effect of Noninnocent Ligands 1748.8 Concluding Remarks 177

References 178

9 Catalytic Function and Mechanism of Heme and Nonheme Iron(IV)–Oxo Complexesin Nature 185Matthew G. Quesne, Abayomi S. Faponle, David P. Goldberg and Sam P. de Visser9.1 Introduction 1859.2 Cytochrome P450 Enzymes 186

9.2.1 Importance of Cytochrome P450 Enzymes 1879.2.2 P450 Activation of Long-Chain Fatty Acids 1889.2.3 Heme Monooxygenases and Peroxygenases 1889.2.4 Catalytic Cycle of Cytochrome P450 Enzymes 188

x Contents

9.3 Nonheme Iron Dioxygenases 1909.3.1 Cysteine Dioxygenase 1919.3.2 AlkB Repair Enzymes 1929.3.3 Nonheme Iron Halogenases 194

9.4 Conclusions 1979.5 Acknowledgments 197

References 197

10 Terminal Metal–Oxo Species with Unusual Spin States 203Sarah A. Cook, David C. Lacy and Andy S. Borovik10.1 Introduction 20310.2 Bonding 204

10.2.1 Bonding Considerations: Tetragonal Symmetry 20410.2.2 Bonding Considerations: Trigonal Symmetry 20510.2.3 Methods of Characterization 206

10.3 Case Studies 20610.3.1 Iron–Oxo Chemistry 20610.3.2 Manganese–Oxo Chemistry 21210.3.3 Cautionary Tales: Late Transition Metal Oxido Complexes 21710.3.4 Effects of Redox Inactive Metal Ions 21710.3.5 Metal–Oxyl Complexes 218

10.4 Reactivity 21810.4.1 General Concepts: Proton versus Electron Transfer 21810.4.2 Spin State and Reactivity 220

10.5 Summary 220References 221

11 Multiple Spin Scenarios in Transition-Metal Complexes Involving RedoxNon-Innocent Ligands 229Florian Heims and Kallol Ray11.1 Introduction 22911.2 Survey of Non-Innocent Ligands 23111.3 Identification of Non-Innocent Ligands 232

11.3.1 X-ray Crystallography 23211.3.2 EPR Spectroscopy 23411.3.3 Mossbauer Spectroscopy 23511.3.4 XAS Spectroscopy 236

11.4 Selected Examples of Biological and Chemical Systems Involving Non-Innocent Ligands 23711.4.1 Copper–Radical Interaction 23711.4.2 Iron–Radical Interaction 246

11.5 Concluding Remarks 252References 253

12 Molecular Magnetism 263Guillem Aromı, Patrick Gamez and Olivier Roubeau12.1 Introduction 26312.2 Molecular Magnetism: Motivations, Early Achievements and Foundations 264

Contents xi

12.3 Molecular Nanomagnets (MNM) 26512.3.1 Single-Molecule Magnets 26612.3.2 Single-Chain Magnets (SCM) 26812.3.3 Single-Ion Magnets (SIM) 271

12.4 Switchable Systems 27312.4.1 Spin Crossover (SCO) 27312.4.2 Valence Tautomerism (VT) 27312.4.3 Charge Transfer (CT) 27512.4.4 Light-Driven Ligand-Induced Spin Change (LD-LISC) 27612.4.5 Photoswitching (PS) Through Intermetallic CT 277

12.5 Molecular-Based Magnetic Refrigerants 27812.5.1 The Magneto-Caloric Effect, Its Experimental Determination and Key Parameters 27812.5.2 Molecular to Extended Framework Coolers Towards Applications 280

12.6 Quantum Manipulation of the Electronic Spin for Quantum Computing 28212.6.1 Organic Radicals 28312.6.2 Transition Metal Clusters 28412.6.3 Lanthanides as Realization of Qubits 28512.6.4 Engineering of Molecular Quantum Gates with Lanthanide Qubits 285

12.7 Perspectives Toward Applications and Concluding Remarks 287References 287

13 Electronic Structure, Bonding, Spin Coupling, and Energetics of Polynuclear Iron–SulfurClusters – A Broken Symmetry Density Functional Theory Perspective 297Kathrin H. Hopmann, Vladimir Pelmenschikov, Wen-Ge Han Du and Louis Noodleman13.1 Introduction 29713.2 Iron–Sulfur Coordination: Geometric and Electronic Structure 29813.3 Spin Polarization Splitting and the Inverted Level Scheme 30013.4 Spin Coupling and the Broken Symmetry Method 30013.5 Electron Localization and Delocalization 30113.6 Polynuclear Systems – Competing Heisenberg Interactions and Spin-Dependent

Delocalization 30313.7 Preamble to Three Major Topics: Iron–Sulfur–Nitrosyls, Adenosine-5′-Phosphosulfate

Reductase, and the Proximal Cluster of Membrane-Bound [NiFe]-Hydrogenase 30313.7.1 Nonheme Iron Nitrosyl Complexes 30313.7.2 Adenosine-5′-Phosphosulfate Reductase 31013.7.3 Proximal Cluster of O2-Tolerant Membrane-Bound [NiFe]-Hydrogenase in Three

Redox States 31513.8 Concluding Remarks 31813.9 Acknowledgments 319

References 319

14 Environment Effects on Spin States, Properties, and Dynamics from Multi-levelQM/MM Studies 327Alexander Petrenko and Matthias Stein14.1 Introduction 327

14.1.1 Environmental Effects 32814.1.2 Hybrid QM/MM Embedding Schemes 329

xii Contents

14.2 The Quantum Spin Hamiltonian – Linking Theory and Experiment 33214.3 The Solvent as an Environment 335

14.3.1 Fourier Transform Infrared Spectroscopy 33614.3.2 Nuclear Magnetic Resonance 33614.3.3 Electron Paramagnetic Resonance 336

14.4 Effect of Different Levels of QM and MM Treatment 33814.4.1 Convergence and Caveats at the QM Level 33814.4.2 Accuracy of the MM Part 34114.4.3 QM versus QM/MM Methods 341

14.5 Illustrative Bioinorganic Examples 34314.5.1 Cytochrome P450 34314.5.2 Hydrogenase Enzymes 34914.5.3 Photosystem II and the Effect of QM Size 354

14.6 From Static Spin-State Properties to Dynamics and Kinetics of Electron Transfer 35714.7 Final Remarks and Conclusions 35914.8 Acknowledgments 362

References 362

15 High-Spin and Low-Spin States in {FeNO}7, FeIV=O, and FeIII–OOH Complexesand Their Correlations to Reactivity 369Edward I. Solomon, Kyle D. Sutherlin and Martin Srnec15.1 Introduction 36915.2 High- and Low-Spin {FeNO}7 Complexes: Correlations to O2 Activation 372

15.2.1 Spectroscopic Definition of the Electronic Structure of High-Spin {FeNO}7 37215.2.2 Computational Studies of S = 3/2 {FeNO}7 Complexes and Related {FeO2}8

Complexes 37515.2.3 Extension to IPNS and HPPD: Implications for Reactivity 37715.2.4 Correlation to {FeNO}7 S = 1/2 385

15.3 Low-Spin (S = 1) and High-Spin (S = 2) FeIV=O Complexes 38615.3.1 FeIV=O S = 1 Complexes: 𝜋∗ FMO 38615.3.2 FeIV=O S = 2 Sites: 𝜋∗ and 𝜎

∗ FMOs 39015.3.3 Contributions of FMOs to Reactivity 392

15.4 Low-Spin (S = 1/2) and High-Spin (S = 5/2) FeIII–OOH Complexes 39615.4.1 Spin State Dependence of O–O Bond Homolysis 39615.4.2 FeIII–OOH S = 1/2 Reactivity: ABLM 39815.4.3 FeIII–OOH Spin State-Dependent Reactivity: FMOs 399

15.5 Concluding Remarks 40115.6 Acknowledgments 402

References 402

16 NMR Analysis of Spin Densities 409Kara L. Bren16.1 Introduction and Scope 40916.2 Spin Density Distribution in Transition Metal Complexes 41016.3 NMR of Paramagnetic Molecules 412

16.3.1 Chemical Shifts 41316.3.2 Relaxation Rates 414

Contents xiii

16.4 Analysis of Spin Densities by NMR 41616.4.1 Factoring Contributions to Hyperfine Shifts 41616.4.2 Relaxation Properties and Spin Density 41816.4.3 DFT Approaches to Analyzing Hyperfine Shifts 41916.4.4 Natural Bond Orbital Analysis 42016.4.5 Application and Practicalities 421

16.5 Probing Spin Densities in Paramagnetic Metalloproteins 42216.5.1 Heme Proteins 42216.5.2 Iron-Sulfur Proteins 42516.5.3 Copper Proteins 427

16.6 Conclusions and Outlook 429References 429

17 Summary and Outlook 435Miquel Costas and Marcel Swart17.1 Summary 43517.2 Outlook 436

References 437

Index 439