Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling

Reed, Christopher J.; Lam, Quan N.; Mirts, Evan N.; Lu, Yi

doi:10.1039/d0cs01297a

Title: Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling

Abstract

Heme-copper oxidases (HCO), nitric oxide reductases (NOR), and sulfite reductases (SiR) catalyze the multi-electron and multi-proton reductions of O₂, NO, and SO₃^2-, respectively. Each of these reactions is important to drive cellular energy production through respiratory metabolism and HCO, NOR, and SiR evolved to contain heteronuclear active sites containing heme/copper, heme/nonheme iron, and heme-[4Fe-4S] centers, respectively. The complexity of the structures and reactions of these native enzymes, along with their large sizes and/or membrane associations, make it challenging to fully understand the crucial structural features responsible for the catalytic properties of these active sites. Here, we summarize progress that has been made to better understand these heteronuclear metalloenzymes at the molecular level though study of the native enzymes along with insights gained from biomimetic models comprising either small molecules or proteins. Further understanding the reaction selectivity of these enzymes is discussed through comparisons of their similar heteronuclear active sites, and we offer outlook for further investigations and areas of ongoing study.

Authors:

^[1]; Lam, Quan N. ^[1]; Mirts, Evan N. ^[1];

^[1]

Univ. of Illinois at Urbana-Champaign, IL (United States)

Publication Date:: Thu Jan 21 00:00:00 EST 2021

Research Org.:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

OSTI Identifier:: 1807581

Alternate Identifier(s):: OSTI ID: 1761247

Grant/Contract Number:: SC0018420; GM062211

Resource Type:: Accepted Manuscript

Journal Name:: Chemical Society Reviews

Additional Journal Information:: Journal Volume: 50; Journal Issue: 4; Journal ID: ISSN 0306-0012

Publisher:: Royal Society of Chemistry

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats


                    Reed, Christopher J., Lam, Quan N., Mirts, Evan N., and Lu, Yi. Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling.  United States: N. p., 2021. 
Web.  doi:10.1039/d0cs01297a.

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                    Reed, Christopher J., Lam, Quan N., Mirts, Evan N., & Lu, Yi. Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling.  United States.  https://doi.org/10.1039/d0cs01297a

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                    Reed, Christopher J., Lam, Quan N., Mirts, Evan N., and Lu, Yi. Thu .  
"Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling".  United States.  https://doi.org/10.1039/d0cs01297a.  https://www.osti.gov/servlets/purl/1807581.

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@article{osti_1807581,

  title        = {Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling},

  author       = {Reed, Christopher J. and Lam, Quan N. and Mirts, Evan N. and Lu, Yi},

  abstractNote = {Heme-copper oxidases (HCO), nitric oxide reductases (NOR), and sulfite reductases (SiR) catalyze the multi-electron and multi-proton reductions of O2, NO, and SO32-, respectively. Each of these reactions is important to drive cellular energy production through respiratory metabolism and HCO, NOR, and SiR evolved to contain heteronuclear active sites containing heme/copper, heme/nonheme iron, and heme-[4Fe-4S] centers, respectively. The complexity of the structures and reactions of these native enzymes, along with their large sizes and/or membrane associations, make it challenging to fully understand the crucial structural features responsible for the catalytic properties of these active sites. Here, we summarize progress that has been made to better understand these heteronuclear metalloenzymes at the molecular level though study of the native enzymes along with insights gained from biomimetic models comprising either small molecules or proteins. Further understanding the reaction selectivity of these enzymes is discussed through comparisons of their similar heteronuclear active sites, and we offer outlook for further investigations and areas of ongoing study.},

  doi          = {10.1039/d0cs01297a},

  journal      = {Chemical Society Reviews},

  number       = 4,

  volume       = 50,

  place        = {United States},

  year         = {Thu Jan 21 00:00:00 EST 2021},

  month        = {Thu Jan 21 00:00:00 EST 2021}

}

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Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 11
DOI: 10.1016/j.bbabio.2017.08.005

Mechanism of Oxygen Reduction in Cytochrome c Oxidase and the Role of the Active Site Tyrosine
journal, January 2016

Blomberg, Margareta R. A.
Biochemistry, Vol. 55, Issue 3
DOI: 10.1021/acs.biochem.5b01205

Intramolecular Proton-Transfer Reactions in a Membrane-Bound Proton Pump: The Effect of pH on the Peroxy to Ferryl Transition in Cytochrome c Oxidase ^† ^, ^⊥
journal, February 2003

Namslauer, Andreas; Aagaard, Anna; Katsonouri, Andromachi
Biochemistry, Vol. 42, Issue 6
DOI: 10.1021/bi026524o

Defining the Proton Entry Point in the Bacterial Respiratory Nitric-oxide Reductase
journal, February 2008

Flock, Ulrika; Thorndycroft, Faye H.; Matorin, Andrey D.
Journal of Biological Chemistry, Vol. 283, Issue 7
DOI: 10.1074/jbc.M704615200

A dedicated haem lyase is required for the maturation of a novel bacterial cytochrome c with unconventional covalent haem binding
journal, May 2007

Hartshorne, Robert S.; Kern, Melanie; Meyer, Björn
Molecular Microbiology, Vol. 64, Issue 4
DOI: 10.1111/j.1365-2958.2007.05712.x

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Title: Molecular understanding of heteronuclear active sites in heme–copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling

Abstract

Citation Formats

The Microbial Engines That Drive Earth's Biogeochemical Cycles journal, May 2008

Bacterial respiration: a flexible process for a changing environment journal, March 2000

Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors journal, July 1997

S- and N-Oxide Reductases journal, April 2007

Diversifying Anaerobic Respiration Strategies to Compete in the Rhizosphere journal, November 2018

Organohalide respiration in pristine environments: implications for the natural halogen cycle: Organohalide respiration in pristine environments journal, December 2017

The antiquity of microbial sulfate reduction journal, February 2004

Denitrification: production and consumption of nitric oxide. journal, January 1994

THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels journal, May 2005

A novel scenario for the evolution of haem–copper oxygen reductases journal, June 2001

The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life journal, March 2006

The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis journal, February 2001

Protein Design: Toward Functional Metalloenzymes journal, January 2014

Artificial Metalloenzymes: Reaction Scope and Optimization Strategies journal, May 2017

Using Biosynthetic Models of Heme-Copper Oxidase and Nitric Oxide Reductase in Myoglobin to Elucidate Structural Features Responsible for Enzymatic Activities journal, September 2016

Understanding and Modulating Metalloenzymes with Unnatural Amino Acids, Non-Native Metal Ions, and Non-Native Metallocofactors journal, March 2019

Engineering Metalloprotein Functions in Designed and Native Scaffolds journal, December 2019

Catalysis and Electron Transfer in De Novo Designed Helical Scaffolds journal, March 2020

Engineering enzymes journal, January 2011

De novo protein design, a retrospective journal, January 2020

Metalloprotein and redox protein design journal, August 2001

Design and engineering of artificial oxygen-activating metalloenzymes journal, January 2016

Dynamics of the K B Proton Pathway in Cytochrome ba 3 from Thermus thermophilus journal, January 2017

Evolution of the haem copper oxidases superfamily: a rooting tale journal, August 2009

A structural and functional perspective on the evolution of the heme-copper oxidases journal, September 2014

Copper Active Sites in Biology journal, January 2014

Functional proton transfer pathways in the heme–copper oxidase superfamily journal, April 2012

Reaction Mechanism of Cytochrome c Oxidase journal, January 2015

Entrance of the proton pathway in cbb3-type heme-copper oxidases journal, October 2011

Substrate binding and the catalytic reactions in cbb3-type oxidases: The lipid membrane modulates ligand binding journal, June 2010

The Diheme Cytochrome c 4 from Vibrio cholerae Is a Natural Electron Donor to the Respiratory cbb 3 Oxygen Reductase journal, September 2010

The Structure of cbb3 Cytochrome Oxidase Provides Insights into Proton Pumping journal, June 2010

Kinetic design of the respiratory oxidases journal, June 2011

Functions of the hydrophilic channels in protonmotive cytochrome c oxidase journal, September 2013

New Perspectives on Proton Pumping in Cellular Respiration journal, February 2015

The Mg 2+ -containing Water Cluster of Mammalian Cytochrome c Oxidase Collects Four Pumping Proton Equivalents in Each Catalytic Cycle journal, September 2016

Cytochrome c oxidase: exciting progress and remaining mysteries journal, October 2008

Proton-transfer pathways in the mitochondrial S. cerevisiae cytochrome c oxidase journal, December 2019

Structure and mechanism of the aberrant ba3-cytochrome c oxidase from Thermus thermophilus journal, April 2000

The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping journal, September 2009

The causes of reduced proton-pumping efficiency in type B and C respiratory heme-copper oxidases, and in some mutated variants of type A journal, July 2014

Oxygen Activation and Energy Conservation by Cytochrome c Oxidase journal, January 2018

Proton pumping by cytochrome c oxidase – A 40 year anniversary journal, September 2018

Proton translocation in cytochrome c oxidase: Insights from proton exchange kinetics and vibrational spectroscopy journal, January 2015

The Whole Structure of the 13-Subunit Oxidized Cytochrome c Oxidase at 2.8 A journal, May 1996

Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans journal, August 1995

Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes journal, February 2013

Mobility of Xe Atoms within the Oxygen Diffusion Channel of Cytochrome ba 3 Oxidase journal, May 2012

Crystallographic Studies of Xe and Kr Binding within the Large Internal Cavity of Cytochrome ba 3 from Thermus thermophilus : Structural Analysis and Role of Oxygen Transport Channels in the Heme−Cu Oxidases † , ‡ journal, April 2008

The X-ray Crystal Structures of Wild-type and EQ(I-286) Mutant Cytochrome c Oxidases from Rhodobacter sphaeroides journal, August 2002

The O2 reduction and proton pumping gate mechanism of bovine heart cytochrome c oxidase journal, October 2011

Bovine cytochrome c oxidase structures enable O 2 reduction with minimization of reactive oxygens and provide a proton-pumping gate journal, April 2010

Broken Symmetry DFT Calculations/Analysis for Oxidized and Reduced Dinuclear Center in Cytochrome c Oxidase: Relating Structures, Protonation States, Energies, and Mössbauer Properties in ba 3 Thermus thermophilus journal, July 2015

Insights into the Functional Role of the Tyrosine−Histidine Linkage in Cytochrome c Oxidase journal, March 2000

Model Studies of the Histidine-Tyrosine Cross-Link in Cytochrome c Oxidase Reveal the Flexible Substituent Effect of the Imidazole Moiety journal, June 2005

Evolutionary Migration of a Post-Translationally Modified Active-Site Residue in the Proton-Pumping Heme-Copper Oxygen Reductases † journal, December 2006

Was nitric oxide the first deep electron sink? journal, January 2009

Structure and Chemistry of Cytochrome P450 journal, June 2005

Synthetic Fe/Cu Complexes: Toward Understanding Heme-Copper Oxidase Structure and Function journal, October 2018

Oxygen Activation and Radical Transformations in Heme Proteins and Metalloporphyrins journal, December 2017

Dioxygen Activation at Mononuclear Nonheme Iron Active Sites: Enzymes, Models, and Intermediates journal, February 2004

Diiron monooxygenases in natural product biosynthesis journal, January 2018

Versatility of biological non-heme Fe(II) centers in oxygen activation reactions journal, February 2008

Multicopper Oxidases and Oxygenases journal, January 1996

The cytochrome bd respiratory oxygen reductases journal, November 2011

Structure of a bd oxidase indicates similar mechanisms for membrane-integrated oxygen reductases journal, April 2016

Cytochrome bd from Azotobacter vinelandii : Evidence for High-Affinity Oxygen Binding † journal, October 2007

Homologous bd oxidases share the same architecture but differ in mechanism journal, November 2019

Discovery of the True Peroxy Intermediate in the Catalytic Cycle of Terminal Oxidases by Real-time Measurement journal, September 2007

Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants journal, March 2013

Unraveling the Heater: New Insights into the Structure of the Alternative Oxidase journal, April 2013

Structure of the trypanosome cyanide-insensitive alternative oxidase journal, March 2013

The alternative oxidases: simple oxidoreductase proteins with complex functions journal, September 2013

Flavo-diiron enzymes: nitric oxide or dioxygen reductases? journal, January 2007

The dual function of flavodiiron proteins: oxygen and/or nitric oxide reductases journal, January 2016

Flavodiiron proteins 1–to-4 function in versatile combinations in O2 photoreduction in cyanobacteria journal, July 2019

Diversity and complexity of flavodiiron NO/O2 reductases journal, December 2017

The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008

Bacterial respiration: a flexible process for a changing environment
journal, March 2000

Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors
journal, July 1997

S- and N-Oxide Reductases
journal, April 2007

Diversifying Anaerobic Respiration Strategies to Compete in the Rhizosphere
journal, November 2018

Organohalide respiration in pristine environments: implications for the natural halogen cycle: Organohalide respiration in pristine environments
journal, December 2017

The antiquity of microbial sulfate reduction
journal, February 2004

Denitrification: production and consumption of nitric oxide.
journal, January 1994

THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels
journal, May 2005

A novel scenario for the evolution of haem–copper oxygen reductases
journal, June 2001

The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life
journal, March 2006

The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis
journal, February 2001

Protein Design: Toward Functional Metalloenzymes
journal, January 2014

Artificial Metalloenzymes: Reaction Scope and Optimization Strategies
journal, May 2017

Using Biosynthetic Models of Heme-Copper Oxidase and Nitric Oxide Reductase in Myoglobin to Elucidate Structural Features Responsible for Enzymatic Activities
journal, September 2016

Understanding and Modulating Metalloenzymes with Unnatural Amino Acids, Non-Native Metal Ions, and Non-Native Metallocofactors
journal, March 2019

Engineering Metalloprotein Functions in Designed and Native Scaffolds
journal, December 2019

Catalysis and Electron Transfer in De Novo Designed Helical Scaffolds
journal, March 2020

Engineering enzymes
journal, January 2011

De novo protein design, a retrospective
journal, January 2020

Metalloprotein and redox protein design
journal, August 2001

Design and engineering of artificial oxygen-activating metalloenzymes
journal, January 2016

Dynamics of the K ^B Proton Pathway in Cytochrome ba ₃ from Thermus thermophilus
journal, January 2017

Evolution of the haem copper oxidases superfamily: a rooting tale
journal, August 2009

A structural and functional perspective on the evolution of the heme-copper oxidases
journal, September 2014

Copper Active Sites in Biology
journal, January 2014

Functional proton transfer pathways in the heme–copper oxidase superfamily
journal, April 2012

Reaction Mechanism of Cytochrome c Oxidase
journal, January 2015

Entrance of the proton pathway in cbb3-type heme-copper oxidases
journal, October 2011

Substrate binding and the catalytic reactions in cbb3-type oxidases: The lipid membrane modulates ligand binding
journal, June 2010

The Diheme Cytochrome c ₄ from Vibrio cholerae Is a Natural Electron Donor to the Respiratory cbb ₃ Oxygen Reductase
journal, September 2010

The Structure of cbb3 Cytochrome Oxidase Provides Insights into Proton Pumping
journal, June 2010

Kinetic design of the respiratory oxidases
journal, June 2011

Functions of the hydrophilic channels in protonmotive cytochrome c oxidase
journal, September 2013

New Perspectives on Proton Pumping in Cellular Respiration
journal, February 2015

The Mg ²⁺ -containing Water Cluster of Mammalian Cytochrome c Oxidase Collects Four Pumping Proton Equivalents in Each Catalytic Cycle
journal, September 2016

Cytochrome c oxidase: exciting progress and remaining mysteries
journal, October 2008

Proton-transfer pathways in the mitochondrial S. cerevisiae cytochrome c oxidase
journal, December 2019

Structure and mechanism of the aberrant ba3-cytochrome c oxidase from Thermus thermophilus
journal, April 2000

The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping
journal, September 2009

The causes of reduced proton-pumping efficiency in type B and C respiratory heme-copper oxidases, and in some mutated variants of type A
journal, July 2014

Oxygen Activation and Energy Conservation by Cytochrome c Oxidase
journal, January 2018

Proton pumping by cytochrome c oxidase – A 40 year anniversary
journal, September 2018

Proton translocation in cytochrome c oxidase: Insights from proton exchange kinetics and vibrational spectroscopy
journal, January 2015

The Whole Structure of the 13-Subunit Oxidized Cytochrome c Oxidase at 2.8 A
journal, May 1996

Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans
journal, August 1995

Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes
journal, February 2013

Mobility of Xe Atoms within the Oxygen Diffusion Channel of Cytochrome ba ₃ Oxidase
journal, May 2012

Crystallographic Studies of Xe and Kr Binding within the Large Internal Cavity of Cytochrome ba ₃ from Thermus thermophilus : Structural Analysis and Role of Oxygen Transport Channels in the Heme−Cu Oxidases ^† ^, ^‡
journal, April 2008

The X-ray Crystal Structures of Wild-type and EQ(I-286) Mutant Cytochrome c Oxidases from Rhodobacter sphaeroides
journal, August 2002

The O2 reduction and proton pumping gate mechanism of bovine heart cytochrome c oxidase
journal, October 2011

Bovine cytochrome c oxidase structures enable O ₂ reduction with minimization of reactive oxygens and provide a proton-pumping gate
journal, April 2010

Broken Symmetry DFT Calculations/Analysis for Oxidized and Reduced Dinuclear Center in Cytochrome c Oxidase: Relating Structures, Protonation States, Energies, and Mössbauer Properties in ba ₃ Thermus thermophilus
journal, July 2015

Insights into the Functional Role of the Tyrosine−Histidine Linkage in Cytochrome c Oxidase
journal, March 2000

Model Studies of the Histidine-Tyrosine Cross-Link in Cytochrome c Oxidase Reveal the Flexible Substituent Effect of the Imidazole Moiety
journal, June 2005

Evolutionary Migration of a Post-Translationally Modified Active-Site Residue in the Proton-Pumping Heme-Copper Oxygen Reductases ^†
journal, December 2006

Was nitric oxide the first deep electron sink?
journal, January 2009

Structure and Chemistry of Cytochrome P450
journal, June 2005

Synthetic Fe/Cu Complexes: Toward Understanding Heme-Copper Oxidase Structure and Function
journal, October 2018

Oxygen Activation and Radical Transformations in Heme Proteins and Metalloporphyrins
journal, December 2017

Dioxygen Activation at Mononuclear Nonheme Iron Active Sites: Enzymes, Models, and Intermediates
journal, February 2004

Diiron monooxygenases in natural product biosynthesis
journal, January 2018

Versatility of biological non-heme Fe(II) centers in oxygen activation reactions
journal, February 2008

Multicopper Oxidases and Oxygenases
journal, January 1996

The cytochrome bd respiratory oxygen reductases
journal, November 2011

Structure of a bd oxidase indicates similar mechanisms for membrane-integrated oxygen reductases
journal, April 2016

Cytochrome bd from Azotobacter vinelandii : Evidence for High-Affinity Oxygen Binding ^†
journal, October 2007

Homologous bd oxidases share the same architecture but differ in mechanism
journal, November 2019

Discovery of the True Peroxy Intermediate in the Catalytic Cycle of Terminal Oxidases by Real-time Measurement
journal, September 2007

Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants
journal, March 2013

Unraveling the Heater: New Insights into the Structure of the Alternative Oxidase
journal, April 2013

Structure of the trypanosome cyanide-insensitive alternative oxidase
journal, March 2013

The alternative oxidases: simple oxidoreductase proteins with complex functions
journal, September 2013

Flavo-diiron enzymes: nitric oxide or dioxygen reductases?
journal, January 2007

The dual function of flavodiiron proteins: oxygen and/or nitric oxide reductases
journal, January 2016

Flavodiiron proteins 1–to-4 function in versatile combinations in O2 photoreduction in cyanobacteria
journal, July 2019

Diversity and complexity of flavodiiron NO/O2 reductases
journal, December 2017

Laccases: a never-ending story
journal, October 2009

Dioxygen Binding, Activation, and Reduction to H ₂ O by Cu Enzymes
journal, June 2016

Mitochondrial cytochrome c oxidase: catalysis, coupling and controversies
journal, June 2017