Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli

Guo, Yirui; Karimullina, Elina; Emde, Tabitha; Otwinowski, Zbyszek; Borek, Dominika; Savchenko, Alexei

doi:10.1002/pro.4616

Title: Monomer and dimer structures of cytochrome bo ₃ ubiquinol oxidase from Escherichia coli

Abstract

Abstract The Escherichia coli cytochrome bo ₃ ubiquinol oxidase is a four‐subunit heme‐copper oxidase that serves as a proton pump in the E. coli aerobic respiratory chain. Despite many mechanistic studies, it is unclear whether this ubiquinol oxidase functions as a monomer, or as a dimer in a manner similar to its eukaryotic counterparts—the mitochondrial electron transport complexes. In this study, we determined the monomeric and dimeric structures of the E. coli cytochrome bo ₃ ubiquinol oxidase reconstituted in amphipol by cryogenic electron microscopy single particle reconstruction (cryo‐EM SPR) to a resolution of 3.15 and 3.46 Å, respectively. We have discovered that the protein can form a dimer with C2 symmetry, with the dimerization interface maintained by interactions between the subunit II of one monomer and the subunit IV of the other monomer. Moreover, the dimerization does not induce significant structural changes in the monomers, except the movement of a loop in subunit IV (residues 67–74).

Authors:

Guo, Yirui ^[1]; Karimullina, Elina ^[2]; Emde, Tabitha ^[3]; Otwinowski, Zbyszek ^[4];

^[4];

^[5]

Department of Biophysics The University of Texas Southwestern Medical Center Dallas Texas USA, Ligo Analytics Dallas Texas USA
Department of Microbiology, Immunology and Infectious Diseases University of Calgary Calgary Alberta Canada, Center for Structural Genomics of Infectious Diseases (CSGID) Chicago Illinois USA, Centers for Research on Structural Biology of Infectious Diseases (CSBID) Chicago Illinois USA
Department of Biophysics The University of Texas Southwestern Medical Center Dallas Texas USA, Center for Structural Genomics of Infectious Diseases (CSGID) Chicago Illinois USA, Centers for Research on Structural Biology of Infectious Diseases (CSBID) Chicago Illinois USA
Department of Biophysics The University of Texas Southwestern Medical Center Dallas Texas USA, Center for Structural Genomics of Infectious Diseases (CSGID) Chicago Illinois USA, Centers for Research on Structural Biology of Infectious Diseases (CSBID) Chicago Illinois USA, Department of Biochemistry The University of Texas Southwestern Medical Center Dallas Texas USA
Department of Microbiology, Immunology and Infectious Diseases University of Calgary Calgary Alberta Canada, Center for Structural Genomics of Infectious Diseases (CSGID) Chicago Illinois USA, Centers for Research on Structural Biology of Infectious Diseases (CSBID) Chicago Illinois USA, BioZone, Department of Chemical Engineering and Applied Chemistry University of Toronto Toronto Ontario Canada

Publication Date:: Fri Mar 24 00:00:00 EDT 2023

Research Org.:: Ligo Analytics, Dallas, TX (United States)

Sponsoring Org.:: USDOE Office of Science (SC); Cancer Prevention and Research Institute of Texas; National Institutes of Health (NIH)

OSTI Identifier:: 1963319

Alternate Identifier(s):: OSTI ID: 1963321; OSTI ID: 1987657

Grant/Contract Number:: DE‐SC0019600; DE‐SC0021600; SC0019600; SC0021600; RP170644; RP220582; 75N93022C00035; HHSN272201700060C; R35GM145365

Resource Type:: Published Article

Journal Name:: Protein Science

Additional Journal Information:: Journal Name: Protein Science Journal Volume: 32 Journal Issue: 4; Journal ID: ISSN 0961-8368

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; cryo-EM; cryogenic electron microscopy; dimer; E. coli cytochrome bo3 ubiquinol oxidase

Citation Formats


                    Guo, Yirui, Karimullina, Elina, Emde, Tabitha, Otwinowski, Zbyszek, Borek, Dominika, and Savchenko, Alexei. Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli.  United Kingdom: N. p., 2023. 
Web.  doi:10.1002/pro.4616.

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                    Guo, Yirui, Karimullina, Elina, Emde, Tabitha, Otwinowski, Zbyszek, Borek, Dominika, & Savchenko, Alexei. Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli.  United Kingdom.  https://doi.org/10.1002/pro.4616

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                    Guo, Yirui, Karimullina, Elina, Emde, Tabitha, Otwinowski, Zbyszek, Borek, Dominika, and Savchenko, Alexei. Fri .  
"Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli".  United Kingdom.  https://doi.org/10.1002/pro.4616.

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@article{osti_1963319,

  title        = {Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli},

  author       = {Guo, Yirui and Karimullina, Elina and Emde, Tabitha and Otwinowski, Zbyszek and Borek, Dominika and Savchenko, Alexei},

  abstractNote = {Abstract The Escherichia coli cytochrome bo 3 ubiquinol oxidase is a four‐subunit heme‐copper oxidase that serves as a proton pump in the E. coli aerobic respiratory chain. Despite many mechanistic studies, it is unclear whether this ubiquinol oxidase functions as a monomer, or as a dimer in a manner similar to its eukaryotic counterparts—the mitochondrial electron transport complexes. In this study, we determined the monomeric and dimeric structures of the E. coli cytochrome bo 3 ubiquinol oxidase reconstituted in amphipol by cryogenic electron microscopy single particle reconstruction (cryo‐EM SPR) to a resolution of 3.15 and 3.46 Å, respectively. We have discovered that the protein can form a dimer with C2 symmetry, with the dimerization interface maintained by interactions between the subunit II of one monomer and the subunit IV of the other monomer. Moreover, the dimerization does not induce significant structural changes in the monomers, except the movement of a loop in subunit IV (residues 67–74).},

  doi          = {10.1002/pro.4616},

  journal      = {Protein Science},

  number       = 4,

  volume       = 32,

  place        = {United Kingdom},

  year         = {Fri Mar 24 00:00:00 EDT 2023},

  month        = {Fri Mar 24 00:00:00 EDT 2023}

}

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Similar Records

Title: Monomer and dimer structures of cytochrome bo 3 ubiquinol oxidase from Escherichia coli

Abstract

Citation Formats

Dimer interface of bovine cytochrome c oxidase is influenced by local posttranslational modifications and lipid binding journal, June 2016

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

Detection of Protein Assemblies in Crystals book, January 2005

Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction journal, November 2020

Cryo-EM structures of Escherichia coli cytochrome bo 3 reveal bound phospholipids and ubiquinone-8 in a dynamic substrate binding site journal, August 2021

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A ‘Build and Retrieve’ methodology to simultaneously solve cryo-EM structures of membrane proteins journal, January 2021

REFMAC 5 for the refinement of macromolecular crystal structures journal, March 2011

Cytochrome o ( bo ) is a proton pump in Paracoccus denitrificans and Escherichia coli journal, June 1989

Artificial intelligence advances for de novo molecular structure modeling in cryo‐electron microscopy journal, May 2021

Structural basis of functions of the mitochondrial cytochrome bc1 complex journal, June 1998

Triton-X-100 induced dissociation of beef heart cytochrome c oxidase into monomers journal, May 1986

The 1.3-Å resolution structure of bovine cytochrome c oxidase suggests a dimerization mechanism journal, January 2021

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix journal, October 2019

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Reaction of the Escherichia coli quinol oxidase cytochrome bo3 with dioxygen: the role of a bound ubiquinone molecule. journal, February 1996

Electron transfer by domain movement in cytochrome bc1 journal, April 1998

Cryo-EM and artificial intelligence visualize endogenous protein community members journal, April 2022

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Evidence for dimer structure of proton-pumping cytochrome c oxidase, an analysis by radiation inactivation. journal, July 1986

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

MOLREP an Automated Program for Molecular Replacement journal, December 1997

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Detergent-solubilized Escherichia coli cytochrome bo 3 ubiquinol oxidase: a monomeric, not a dimeric complex journal, August 1999

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Title: Monomer and dimer structures of cytochrome bo ₃ ubiquinol oxidase from Escherichia coli

Dimer interface of bovine cytochrome c oxidase is influenced by local posttranslational modifications and lipid binding
journal, June 2016

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

Detection of Protein Assemblies in Crystals
book, January 2005

Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction
journal, November 2020

Cryo-EM structures of Escherichia coli cytochrome bo ₃ reveal bound phospholipids and ubiquinone-8 in a dynamic substrate binding site
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MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

Cryo-EM single-particle structure refinement and map calculation usingServalcat
journal, September 2021

Coot model-building tools for molecular graphics
journal, November 2004

Features and development of Coot
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A ‘Build and Retrieve’ methodology to simultaneously solve cryo-EM structures of membrane proteins
journal, January 2021

REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011

Cytochrome o ( bo ) is a proton pump in Paracoccus denitrificans and Escherichia coli
journal, June 1989

Artificial intelligence advances for de novo molecular structure modeling in cryo‐electron microscopy
journal, May 2021

Structural basis of functions of the mitochondrial cytochrome bc1 complex
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Triton-X-100 induced dissociation of beef heart cytochrome c oxidase into monomers
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The 1.3-Å resolution structure of bovine cytochrome c oxidase suggests a dimerization mechanism
journal, January 2021

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
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Cryo-EM structure provides insights into the dimer arrangement of the O-linked β-N-acetylglucosamine transferase OGT
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Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions
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Reaction of the Escherichia coli quinol oxidase cytochrome bo3 with dioxygen: the role of a bound ubiquinone molecule.
journal, February 1996

Electron transfer by domain movement in cytochrome bc1
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Cryo-EM and artificial intelligence visualize endogenous protein community members
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Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions
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Evidence for dimer structure of proton-pumping cytochrome c oxidase, an analysis by radiation inactivation.
journal, July 1986

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

MOLREP an Automated Program for Molecular Replacement
journal, December 1997

Real-space refinement in PHENIX for cryo-EM and crystallography
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journal, September 2007

Automated electron microscope tomography using robust prediction of specimen movements
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