Viscous control of cellular respiration by membrane lipid composition

Budin, Itay; de Rond, Tristan; Chen, Yan; Chan, Leanne Jade G.; Petzold, Christopher J.; Keasling, Jay D.

doi:10.1126/science.aat7925

Title: Viscous control of cellular respiration by membrane lipid composition

Abstract

Lipid composition determines the physical properties of biological membranes and can vary substantially between and within organisms. We describe a specific role for the viscosity of energy-transducing membranes in cellular respiration. Engineering of fatty acid biosynthesis in Escherichia coli allowed us to titrate inner membrane viscosity across a 10-fold range by controlling the abundance of unsaturated or branched lipids. These fluidizing lipids tightly controlled respiratory metabolism, an effect that can be explained with a quantitative model of the electron transport chain (ETC) that features diffusion-coupled reactions between enzymes and electron carriers (quinones). Lipid unsaturation also modulated mitochondrial respiration in engineered budding yeast strains. Thus, diffusion in the ETC may serve as an evolutionary constraint for lipid composition in respiratory membranes.

Authors:

;

; Chan, Leanne Jade G.;

;

Publication Date:: Thu Oct 25 00:00:00 EDT 2018

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC)

OSTI Identifier:: 1484838

Alternate Identifier(s):: OSTI ID: 1656478

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Science

Additional Journal Information:: Journal Name: Science Journal Volume: 362 Journal Issue: 6419; Journal ID: ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Budin, Itay, de Rond, Tristan, Chen, Yan, Chan, Leanne Jade G., Petzold, Christopher J., and Keasling, Jay D. Viscous control of cellular respiration by membrane lipid composition.  United States: N. p., 2018. 
Web.  doi:10.1126/science.aat7925.

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                    Budin, Itay, de Rond, Tristan, Chen, Yan, Chan, Leanne Jade G., Petzold, Christopher J., & Keasling, Jay D. Viscous control of cellular respiration by membrane lipid composition.  United States.  https://doi.org/10.1126/science.aat7925

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                    Budin, Itay, de Rond, Tristan, Chen, Yan, Chan, Leanne Jade G., Petzold, Christopher J., and Keasling, Jay D. Thu .  
"Viscous control of cellular respiration by membrane lipid composition".  United States.  https://doi.org/10.1126/science.aat7925.

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@article{osti_1484838,

  title        = {Viscous control of cellular respiration by membrane lipid composition},

  author       = {Budin, Itay and de Rond, Tristan and Chen, Yan and Chan, Leanne Jade G. and Petzold, Christopher J. and Keasling, Jay D.},

  abstractNote = {Lipid composition determines the physical properties of biological membranes and can vary substantially between and within organisms. We describe a specific role for the viscosity of energy-transducing membranes in cellular respiration. Engineering of fatty acid biosynthesis in Escherichia coli allowed us to titrate inner membrane viscosity across a 10-fold range by controlling the abundance of unsaturated or branched lipids. These fluidizing lipids tightly controlled respiratory metabolism, an effect that can be explained with a quantitative model of the electron transport chain (ETC) that features diffusion-coupled reactions between enzymes and electron carriers (quinones). Lipid unsaturation also modulated mitochondrial respiration in engineered budding yeast strains. Thus, diffusion in the ETC may serve as an evolutionary constraint for lipid composition in respiratory membranes.},

  doi          = {10.1126/science.aat7925},

  journal      = {Science},

  number       = 6419,

  volume       = 362,

  place        = {United States},

  year         = {Thu Oct 25 00:00:00 EDT 2018},

  month        = {Thu Oct 25 00:00:00 EDT 2018}

}

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Title: Viscous control of cellular respiration by membrane lipid composition

Abstract

Citation Formats

The Enigma of the Respiratory Chain Supercomplex journal, April 2017

Thermal Adaptation in Biological Membranes: Is Homeoviscous Adaptation the Explanation? journal, October 1995

Independent mobility of proteins and lipids in the plasma membrane of E scherichia coli : Protein diffusion in a bacterial plasma membrane journal, April 2014

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Escherichia coli Unsaturated Fatty Acid Synthesis: COMPLEX TRANSCRIPTION OF THE fabA GENE AND IN VIVO IDENTIFICATION OF THE ESSENTIAL REACTION CATALYZED BY FabB journal, August 2009

The effect of diffusion on the binding of membrane-bound receptors to coated pits journal, January 1985

Regulation of the heat-shock response journal, April 1999

Panorama: A Targeted Proteomics Knowledge Base journal, July 2014

Lateral mobility of proteins in liquid membranes revisited journal, February 2006

Homeoviscous Adaptation--A Homeostatic Process that Regulates the Viscosity of Membrane Lipids in Escherichia coli journal, February 1974

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Electrochemical Measurement of Lateral Diffusion Coefficients of Ubiquinones and Plastoquinones of Various Isoprenoid Chain Lengths Incorporated in Model Bilayers journal, April 1998

Adaptations to energy stress dictate the ecology and evolution of the Archaea journal, March 2007

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Tuning genetic control through promoter engineering journal, August 2005

Membrane lipids: where they are and how they behave journal, February 2008

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A targeted proteomics toolkit for high-throughput absolute quantification of Escherichia coli proteins journal, November 2014

Clustering and dynamics of cytochrome bd -I complexes in the Escherichia coli plasma membrane in vivo journal, December 2008

Diffusion of Liquid Domains in Lipid Bilayer Membranes journal, April 2007

Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batch-culture growth journal, June 2007

The Escherichia coli CydX Protein Is a Member of the CydAB Cytochrome bd Oxidase Complex and Is Required for Cytochrome bd Oxidase Activity journal, June 2013

Homogeneous expression of the PBAD promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter journal, December 2001

Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile journal, April 1991

Lipid engineering reveals regulatory roles for membrane fluidity in yeast flocculation and oxygen-limited growth journal, May 2017

Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbruck equations. journal, July 1982

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Understanding the Role of Mitochondrial Health in the Mechanism of Mitochondrial Bioelectrocatalysis journal, January 2016

Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation journal, June 2014

High Throughput Microplate Respiratory Measurements Using Minimal Quantities Of Isolated Mitochondria journal, July 2011

Kinetic evidence against partitioning of the ubiquinone pool and the catalytic relevance of respiratory-chain supercomplexes journal, October 2014

Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode journal, October 2011

Supercomplex Assembly Determines Electron Flux in the Mitochondrial Electron Transport Chain journal, June 2013

The architecture of respiratory supercomplexes journal, September 2016

Respiratory Control in Escherichia coli K 12 journal, March 1979

A generalised model for the equilibration of quinone pools with their biological donors and acceptors in membrane-bound electron transfer chains journal, August 1981

Brownian motion in biological membranes. journal, August 1975

Green Fluorescent Protein as a Noninvasive Stress Probe in Resting Escherichia coli Cells journal, February 1999

Generation of giant protoplasts of Escherichia coli and an inner-membrane anion selective conductance journal, September 1995

Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli journal, July 1999

Relationship between lateral diffusion, collision frequency, and electron transfer of mitochondrial inner membrane oxidation-reduction components. journal, May 1984

Arrangement of electron transport chain components in bovine mitochondrial supercomplex I 1 III 2 IV 1 : Cryo-EM of respiratory chain supercomplex journal, September 2011

The Mitochondrial Respiratory Chain Is Partially Organized in a Supercomplex Assembly: KINETIC EVIDENCE USING FLUX CONTROL ANALYSIS journal, June 2004

Understanding the diversity of membrane lipid composition journal, February 2018

Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues journal, February 2000

A Eukaryotic Sensor for Membrane Lipid Saturation journal, July 2016

A calorimetric and fluorescent probe study of the gel-liquid crystalline phase transition in small, single-lamellar dipalmitoylphosphatidylcholine vesicles journal, April 1976

Escherichia coli FadR Positively Regulates Transcription of the fabB Fatty Acid Biosynthetic Gene journal, October 2001

Assay of Succinate Dehydrogenase Activity by a Colorimetric-Continuous Method Using Iodonitrotetrazolium Chloride as Electron Acceptor journal, August 1993

Determination of partition and lateral diffusion coefficients of ubiquinones by fluorescence quenching of n-(9-anthroyloxy)stearic acids in phospholipid vesicles and mitochondrial membranes journal, June 1986

17β-Estradiol Directly Lowers Mitochondrial Membrane Microviscosity and Improves Bioenergetic Function in Skeletal Muscle journal, January 2018

Role of diffusion in ligand binding to macromolecules and cell-bound receptors journal, October 1982

Lateral diffusion in biological membranes. A normal-mode analysis of diffusion on a spherical surface journal, April 1980

NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain journal, December 1987

LipidXplorer: A Software for Consensual Cross-Platform Lipidomics journal, January 2012

Precise determination of the hydrodynamic radius of phospholipid vesicles near the phase transition journal, November 1984

Fumarate Reductase and Succinate Oxidase Activity of Escherichia coli Complex II Homologs Are Perturbed Differently by Mutation of the Flavin Binding Domain journal, February 2006

The Enigma of the Respiratory Chain Supercomplex
journal, April 2017

Thermal Adaptation in Biological Membranes: Is Homeoviscous Adaptation the Explanation?
journal, October 1995

Independent mobility of proteins and lipids in the plasma membrane of E scherichia coli : Protein diffusion in a bacterial plasma membrane
journal, April 2014

Reduced Flavins Promote Oxidative DNA Damage in Non-respiring Escherichia coli by Delivering Electrons to Intracellular Free Iron
journal, June 2002

Characterization of the Overproduced NADH Dehydrogenase Fragment of the NADH:Ubiquinone Oxidoreductase (Complex I) from Escherichia coli ^†
journal, February 1998

Escherichia coli Unsaturated Fatty Acid Synthesis: COMPLEX TRANSCRIPTION OF THE fabA GENE AND IN VIVO IDENTIFICATION OF THE ESSENTIAL REACTION CATALYZED BY FabB
journal, August 2009

The effect of diffusion on the binding of membrane-bound receptors to coated pits
journal, January 1985

Regulation of the heat-shock response
journal, April 1999

Panorama: A Targeted Proteomics Knowledge Base
journal, July 2014

Lateral mobility of proteins in liquid membranes revisited
journal, February 2006

Homeoviscous Adaptation--A Homeostatic Process that Regulates the Viscosity of Membrane Lipids in Escherichia coli
journal, February 1974

Production of anteiso-branched fatty acids in Escherichia coli; next generation biofuels with improved cold-flow properties
journal, November 2014

Electrochemical Measurement of Lateral Diffusion Coefficients of Ubiquinones and Plastoquinones of Various Isoprenoid Chain Lengths Incorporated in Model Bilayers
journal, April 1998

Adaptations to energy stress dictate the ecology and evolution of the Archaea
journal, March 2007

A robust system for production of minicircle DNA vectors
journal, November 2010

Effect of Hydrodynamic Interactions on Reaction Rates in Membranes
journal, July 2017

Tuning genetic control through promoter engineering
journal, August 2005

Membrane lipids: where they are and how they behave
journal, February 2008

Investigation of diffusion-limited rates of chymotrypsin reactions by viscosity variation
journal, March 1982

A targeted proteomics toolkit for high-throughput absolute quantification of Escherichia coli proteins
journal, November 2014

Clustering and dynamics of cytochrome bd -I complexes in the Escherichia coli plasma membrane in vivo
journal, December 2008

Diffusion of Liquid Domains in Lipid Bilayer Membranes
journal, April 2007

Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batch-culture growth
journal, June 2007

The Escherichia coli CydX Protein Is a Member of the CydAB Cytochrome bd Oxidase Complex and Is Required for Cytochrome bd Oxidase Activity
journal, June 2013

Homogeneous expression of the PBAD promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter
journal, December 2001

Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile
journal, April 1991

Lipid engineering reveals regulatory roles for membrane fluidity in yeast flocculation and oxygen-limited growth
journal, May 2017

Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbruck equations.
journal, July 1982

Physics of chemoreception
journal, November 1977

Understanding the Role of Mitochondrial Health in the Mechanism of Mitochondrial Bioelectrocatalysis
journal, January 2016

Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation
journal, June 2014

High Throughput Microplate Respiratory Measurements Using Minimal Quantities Of Isolated Mitochondria
journal, July 2011

Kinetic evidence against partitioning of the ubiquinone pool and the catalytic relevance of respiratory-chain supercomplexes
journal, October 2014

Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode
journal, October 2011

Supercomplex Assembly Determines Electron Flux in the Mitochondrial Electron Transport Chain
journal, June 2013

The architecture of respiratory supercomplexes
journal, September 2016

Respiratory Control in Escherichia coli K 12
journal, March 1979

A generalised model for the equilibration of quinone pools with their biological donors and acceptors in membrane-bound electron transfer chains
journal, August 1981

Brownian motion in biological membranes.
journal, August 1975

Green Fluorescent Protein as a Noninvasive Stress Probe in Resting Escherichia coli Cells
journal, February 1999

Generation of giant protoplasts of Escherichia coli and an inner-membrane anion selective conductance
journal, September 1995

Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli
journal, July 1999

Relationship between lateral diffusion, collision frequency, and electron transfer of mitochondrial inner membrane oxidation-reduction components.
journal, May 1984

Arrangement of electron transport chain components in bovine mitochondrial supercomplex I ₁ III ₂ IV ₁ : Cryo-EM of respiratory chain supercomplex
journal, September 2011

The Mitochondrial Respiratory Chain Is Partially Organized in a Supercomplex Assembly: KINETIC EVIDENCE USING FLUX CONTROL ANALYSIS
journal, June 2004

Understanding the diversity of membrane lipid composition
journal, February 2018

Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues
journal, February 2000

A Eukaryotic Sensor for Membrane Lipid Saturation
journal, July 2016

A calorimetric and fluorescent probe study of the gel-liquid crystalline phase transition in small, single-lamellar dipalmitoylphosphatidylcholine vesicles
journal, April 1976

Escherichia coli FadR Positively Regulates Transcription of the fabB Fatty Acid Biosynthetic Gene
journal, October 2001

Assay of Succinate Dehydrogenase Activity by a Colorimetric-Continuous Method Using Iodonitrotetrazolium Chloride as Electron Acceptor
journal, August 1993

Determination of partition and lateral diffusion coefficients of ubiquinones by fluorescence quenching of n-(9-anthroyloxy)stearic acids in phospholipid vesicles and mitochondrial membranes
journal, June 1986

17β-Estradiol Directly Lowers Mitochondrial Membrane Microviscosity and Improves Bioenergetic Function in Skeletal Muscle
journal, January 2018

Role of diffusion in ligand binding to macromolecules and cell-bound receptors
journal, October 1982

Lateral diffusion in biological membranes. A normal-mode analysis of diffusion on a spherical surface
journal, April 1980

NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain
journal, December 1987

LipidXplorer: A Software for Consensual Cross-Platform Lipidomics
journal, January 2012

Precise determination of the hydrodynamic radius of phospholipid vesicles near the phase transition
journal, November 1984

Fumarate Reductase and Succinate Oxidase Activity of Escherichia coli Complex II Homologs Are Perturbed Differently by Mutation of the Flavin Binding Domain
journal, February 2006