β-Barrel proteins tether the outer membrane in many Gram-negative bacteria

Sandoz, Kelsi M.; Moore, Roger A.; Beare, Paul A.; Patel, Ankur V.; Smith, Robert E.; Bern, Marshall; Hwang, Hyea; Cooper, Connor J.; Priola, Suzette A.; Parks, Jerry M.; Gumbart, James C.; Mesnage, Stéphane; Heinzen, Robert A.

doi:10.1038/s41564-020-00798-4

Title: β-Barrel proteins tether the outer membrane in many Gram-negative bacteria

Abstract

Gram-negative bacteria have a cell envelope that comprises an outer membrane (OM), a peptidoglycan (PG) layer and an inner membrane (IM). The OM and PG are load-bearing, selectively permeable structures that are stabilized by cooperative interactions between IM and OM proteins. In Escherichia coli, Braun’s lipoprotein (Lpp) forms the only covalent tether between the OM and PG and is crucial for cell envelope stability; however, most other Gram-negative bacteria lack Lpp so it has been assumed that alternative mechanisms of OM stabilization are present. In this work we used a glycoproteomic analysis of PG to show that β-barrel OM proteins are covalently attached to PG in several Gram-negative species, including Coxiella burnetii, Agrobacterium tumefaciens and Legionella pneumophila. In C. burnetii, we found that four different types of covalent attachments occur between OM proteins and PG, with tethering of the β-barrel OM protein BbpA becoming most abundant in the stationary phase and tethering of the lipoprotein LimB similar throughout the cell cycle. Using a genetic approach, we demonstrate that the cell cycle-dependent tethering of BbpA is partly dependent on a developmentally regulated L,D-transpeptidase (Ldt). We use our findings to propose a model of Gram-negative cell envelope stabilization that includes cell cyclemore »« less

Authors:

^[1]; Moore, Roger A. ^[1]; Beare, Paul A. ^[1];

^[2]; Smith, Robert E. ^[2];

^[3]; Hwang, Hyea ^[4];

^[5]; Priola, Suzette A. ^[1];

^[5]; Gumbart, James C. ^[4];

^[2];

^[1]

National Inst. of Health (NIH), Hamilton, MT (United States). National Inst. of Allergy and Infectious Diseases (NIAID)
Univ. of Sheffield (United Kingdom)
Protein Metrics Inc., Cupertino, CA (United States)
Georgia Inst. of Technology, Atlanta, GA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)

Publication Date:: Mon Nov 02 00:00:00 EST 2020

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Compute and Data Environment for Science (CADES)

Sponsoring Org.:: National Institutes of Health (NIH); National Institute of Allergy and Infectious Diseases (NIAID); Medical Research Council (MRC); Biotechnology and Biological Sciences Research Council (BBSRC); National Science Foundation (NSF); USDOE Laboratory Directed Research and Development (LDRD) Program

OSTI Identifier:: 1706272

Grant/Contract Number:: AC05-00OR22725; MR/S009272/1; BBSRC BB/N000951/1; BB/M011151/1; R01-GM123169; 2017219379; ACI-1548562

Resource Type:: Accepted Manuscript

Journal Name:: Nature Microbiology

Additional Journal Information:: Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2058-5276

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Bacterial pathogenesis; Bacterial structural biology

Citation Formats


                    Sandoz, Kelsi M., Moore, Roger A., Beare, Paul A., Patel, Ankur V., Smith, Robert E., Bern, Marshall, Hwang, Hyea, Cooper, Connor J., Priola, Suzette A., Parks, Jerry M., Gumbart, James C., Mesnage, Stéphane, and Heinzen, Robert A. β-Barrel proteins tether the outer membrane in many Gram-negative bacteria.  United States: N. p., 2020. 
Web.  doi:10.1038/s41564-020-00798-4.

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                    Sandoz, Kelsi M., Moore, Roger A., Beare, Paul A., Patel, Ankur V., Smith, Robert E., Bern, Marshall, Hwang, Hyea, Cooper, Connor J., Priola, Suzette A., Parks, Jerry M., Gumbart, James C., Mesnage, Stéphane, & Heinzen, Robert A. β-Barrel proteins tether the outer membrane in many Gram-negative bacteria.  United States.  https://doi.org/10.1038/s41564-020-00798-4

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                    Sandoz, Kelsi M., Moore, Roger A., Beare, Paul A., Patel, Ankur V., Smith, Robert E., Bern, Marshall, Hwang, Hyea, Cooper, Connor J., Priola, Suzette A., Parks, Jerry M., Gumbart, James C., Mesnage, Stéphane, and Heinzen, Robert A. Mon .  
"β-Barrel proteins tether the outer membrane in many Gram-negative bacteria".  United States.  https://doi.org/10.1038/s41564-020-00798-4.  https://www.osti.gov/servlets/purl/1706272.

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@article{osti_1706272,

  title        = {β-Barrel proteins tether the outer membrane in many Gram-negative bacteria},

  author       = {Sandoz, Kelsi M. and Moore, Roger A. and Beare, Paul A. and Patel, Ankur V. and Smith, Robert E. and Bern, Marshall and Hwang, Hyea and Cooper, Connor J. and Priola, Suzette A. and Parks, Jerry M. and Gumbart, James C. and Mesnage, Stéphane and Heinzen, Robert A.},

  abstractNote = {Gram-negative bacteria have a cell envelope that comprises an outer membrane (OM), a peptidoglycan (PG) layer and an inner membrane (IM). The OM and PG are load-bearing, selectively permeable structures that are stabilized by cooperative interactions between IM and OM proteins. In Escherichia coli, Braun’s lipoprotein (Lpp) forms the only covalent tether between the OM and PG and is crucial for cell envelope stability; however, most other Gram-negative bacteria lack Lpp so it has been assumed that alternative mechanisms of OM stabilization are present. In this work we used a glycoproteomic analysis of PG to show that β-barrel OM proteins are covalently attached to PG in several Gram-negative species, including Coxiella burnetii, Agrobacterium tumefaciens and Legionella pneumophila. In C. burnetii, we found that four different types of covalent attachments occur between OM proteins and PG, with tethering of the β-barrel OM protein BbpA becoming most abundant in the stationary phase and tethering of the lipoprotein LimB similar throughout the cell cycle. Using a genetic approach, we demonstrate that the cell cycle-dependent tethering of BbpA is partly dependent on a developmentally regulated L,D-transpeptidase (Ldt). We use our findings to propose a model of Gram-negative cell envelope stabilization that includes cell cycle control and an expanded role for Ldts in covalently attaching surface proteins to PG.},

  doi          = {10.1038/s41564-020-00798-4},

  journal      = {Nature Microbiology},

  number       = 1,

  volume       = 6,

  place        = {United States},

  year         = {Mon Nov 02 00:00:00 EST 2020},

  month        = {Mon Nov 02 00:00:00 EST 2020}

}

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Title: β-Barrel proteins tether the outer membrane in many Gram-negative bacteria

Abstract

Citation Formats

Bacterial outer membrane constriction: Outer membrane constriction journal, January 2018

Sequence of the Murein . Lipoprotein and the Attachment Site of the Lipid journal, June 1972

The Bacterial Cell Envelope journal, April 2010

Scalable molecular dynamics with NAMD journal, January 2005

Protein homology detection by HMM-HMM comparison journal, November 2004

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Chemical Characterization, Spatial Distribution and Function of a Lipoprotein (Murein-Lipoprotein) of the E. coli Cell Wall. The Specific Effect of Trypsin on the Membrane Structure journal, October 1969

Covalent lipoprotein from the outer membrane of escherichia coli journal, October 1975

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Microbe-Host Interactions: Structure and Role of Gram-Negative Bacterial Porins journal, December 2012

The Life Cycle of L. pneumophila: Cellular Differentiation Is Linked to Virulence and Metabolism journal, January 2018

Transcriptional Profiling of Coxiella burnetii Reveals Extensive Cell Wall Remodeling in the Small Cell Variant Developmental Form journal, February 2016

Assessing the utility of coevolution-based residue-residue contact predictions in a sequence- and structure-rich era journal, September 2013

OmpA: A Flexible Clamp for Bacterial Cell Wall Attachment journal, December 2016

Peptidoglycan-associated lipoprotein (Pal) of Gram-negative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis journal, September 2009

Communication across the bacterial cell envelope depends on the size of the periplasm journal, December 2017

The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria journal, November 2008

Characterization of a major 31-kilodalton peptidoglycan-bound protein of Legionella pneumophila. journal, January 1990

Protein structure determination using metagenome sequence data journal, January 2017

Don’t let sleeping dogmas lie: new views of peptidoglycan synthesis and its regulation: New views on peptdigoglycan synthesis journal, October 2017

Two Systems for Targeted Gene Deletion in Coxiella burnetii journal, April 2012

Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane journal, January 2012

Complementation of Arginine Auxotrophy for Genetic Transformation of Coxiella burnetii by Use of a Defined Axenic Medium journal, March 2016

Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types journal, June 2010

Lag Phase Is a Dynamic, Organized, Adaptive, and Evolvable Period That Prepares Bacteria for Cell Division journal, January 2019

CHARMM36m: an improved force field for folded and intrinsically disordered proteins journal, November 2016

Nanoscale-length control of the flagellar driveshaft requires hitting the tethered outer membrane journal, April 2017

Outer membrane permeability and antibiotic resistance journal, May 2009

Ecological and evolutionary dynamics of a model facultative pathogen: Agrobacterium and crown gall disease of plants: Evolutionary ecology of crown gall disease journal, December 2017

Lpp, the Braun lipoprotein, turns 50—major achievements and remaining issues journal, August 2018

Stimulation of Toll-like Receptor 2 by Coxiella burnetii Is Required for Macrophage Production of Pro-inflammatory Cytokines and Resistance to Infection journal, October 2004

A unique Coxiella burnetii lipoprotein involved in metal binding (LimB) journal, April 2011

Peptidoglycan Remodeling Enables Escherichia coli To Survive Severe Outer Membrane Assembly Defect journal, February 2019

Peptidoglycan of Legionella pneumophila: apparent resistance to lysozyme hydrolysis correlates with a high degree of peptide cross-linking. journal, January 1983

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems journal, June 1993

UniProt: a worldwide hub of protein knowledge November 2018

Learning generative models for protein fold families journal, January 2011

Sensitivity of Coxiella burnetii peptidoglycan to lysozyme hydrolysis and correlation of sacculus rigidity with peptidoglycan-associated proteins. journal, January 1984

Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. journal, January 1978

Towards an automated analysis of bacterial peptidoglycan structure journal, August 2016

The outer membrane is an essential load-bearing element in Gram-negative bacteria journal, July 2018

Partial Characterization of Peptidoglycan-Associated Proteins of Legionella pneumophila1 journal, July 1983

Escherichia coli Peptidoglycan Structure and Mechanics as Predicted by Atomic-Scale Simulations journal, February 2014

HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment journal, December 2011

Identification of the L,D-Transpeptidases for Peptidoglycan Cross-Linking in Escherichia coli journal, May 2008

The Murein-Lipoprotein Linkage in the Cell Wall of Escherichia coli journal, June 1970

Distribution of mechanical stress in the Escherichia coli cell envelope journal, December 2018

Crystal Structure of Neisserial Surface Protein A (NspA), a Conserved Outer Membrane Protein with Vaccine Potential journal, April 2003

[18] Genetic Analysis of Agrobacterium book, January 1991

A Coxiella burnetii phospholipase A homolog pldA is required for optimal growth in macrophages and developmental form lipid remodeling journal, April 2018

Living on the edge: Simulations of bacterial outer-membrane proteins journal, July 2016

High-resolution structure of the OmpA membrane domain journal, April 2000

Identification of the l,d-Transpeptidases Responsible for Attachment of the Braun Lipoprotein to Escherichia coli Peptidoglycan journal, March 2007

VMD: Visual molecular dynamics journal, February 1996

The physiology of growth arrest: uniting molecular and environmental microbiology journal, August 2016

Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations. journal, January 1981

Bacterial outer membrane constriction: Outer membrane constriction
journal, January 2018

Sequence of the Murein . Lipoprotein and the Attachment Site of the Lipid
journal, June 1972

The Bacterial Cell Envelope
journal, April 2010

Scalable molecular dynamics with NAMD
journal, January 2005

Protein homology detection by HMM-HMM comparison
journal, November 2004

Molecular characterization of the 28- and 31-kilodalton subunits of the Legionella pneumophila major outer membrane protein.
journal, January 1992

High-Resolution Comparative Modeling with RosettaCM
journal, October 2013

Peptidoglycan Cross-Linking Activity of L,D-Transpeptidases from Clostridium difficile and Inactivation of These Enzymes by β-Lactams
journal, October 2017

OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar
journal, May 2008

Chemical Characterization, Spatial Distribution and Function of a Lipoprotein (Murein-Lipoprotein) of the E. coli Cell Wall. The Specific Effect of Trypsin on the Membrane Structure
journal, October 1969

Covalent lipoprotein from the outer membrane of escherichia coli
journal, October 1975

A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core
journal, July 2018

Microbe-Host Interactions: Structure and Role of Gram-Negative Bacterial Porins
journal, December 2012

The Life Cycle of L. pneumophila: Cellular Differentiation Is Linked to Virulence and Metabolism
journal, January 2018

Transcriptional Profiling of Coxiella burnetii Reveals Extensive Cell Wall Remodeling in the Small Cell Variant Developmental Form
journal, February 2016

Assessing the utility of coevolution-based residue-residue contact predictions in a sequence- and structure-rich era
journal, September 2013

OmpA: A Flexible Clamp for Bacterial Cell Wall Attachment
journal, December 2016

Peptidoglycan-associated lipoprotein (Pal) of Gram-negative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis
journal, September 2009

Communication across the bacterial cell envelope depends on the size of the periplasm
journal, December 2017

The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria
journal, November 2008

Characterization of a major 31-kilodalton peptidoglycan-bound protein of Legionella pneumophila.
journal, January 1990

Protein structure determination using metagenome sequence data
journal, January 2017

Don’t let sleeping dogmas lie: new views of peptidoglycan synthesis and its regulation: New views on peptdigoglycan synthesis
journal, October 2017

Two Systems for Targeted Gene Deletion in Coxiella burnetii
journal, April 2012

Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane
journal, January 2012

Complementation of Arginine Auxotrophy for Genetic Transformation of Coxiella burnetii by Use of a Defined Axenic Medium
journal, March 2016

Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types
journal, June 2010

Lag Phase Is a Dynamic, Organized, Adaptive, and Evolvable Period That Prepares Bacteria for Cell Division
journal, January 2019

CHARMM36m: an improved force field for folded and intrinsically disordered proteins
journal, November 2016

Nanoscale-length control of the flagellar driveshaft requires hitting the tethered outer membrane
journal, April 2017

Outer membrane permeability and antibiotic resistance
journal, May 2009

Ecological and evolutionary dynamics of a model facultative pathogen: Agrobacterium and crown gall disease of plants: Evolutionary ecology of crown gall disease
journal, December 2017

Lpp, the Braun lipoprotein, turns 50—major achievements and remaining issues
journal, August 2018

Stimulation of Toll-like Receptor 2 by Coxiella burnetii Is Required for Macrophage Production of Pro-inflammatory Cytokines and Resistance to Infection
journal, October 2004

A unique Coxiella burnetii lipoprotein involved in metal binding (LimB)
journal, April 2011

Peptidoglycan Remodeling Enables Escherichia coli To Survive Severe Outer Membrane Assembly Defect
journal, February 2019

Peptidoglycan of Legionella pneumophila: apparent resistance to lysozyme hydrolysis correlates with a high degree of peptide cross-linking.
journal, January 1983

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993

UniProt: a worldwide hub of protein knowledge
November 2018

Learning generative models for protein fold families
journal, January 2011

Sensitivity of Coxiella burnetii peptidoglycan to lysozyme hydrolysis and correlation of sacculus rigidity with peptidoglycan-associated proteins.
journal, January 1984

Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins.
journal, January 1978

Towards an automated analysis of bacterial peptidoglycan structure
journal, August 2016

The outer membrane is an essential load-bearing element in Gram-negative bacteria
journal, July 2018

Partial Characterization of Peptidoglycan-Associated Proteins of Legionella pneumophila1
journal, July 1983

Escherichia coli Peptidoglycan Structure and Mechanics as Predicted by Atomic-Scale Simulations
journal, February 2014

HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment
journal, December 2011

Identification of the L,D-Transpeptidases for Peptidoglycan Cross-Linking in Escherichia coli
journal, May 2008

The Murein-Lipoprotein Linkage in the Cell Wall of Escherichia coli
journal, June 1970

Distribution of mechanical stress in the Escherichia coli cell envelope
journal, December 2018

Crystal Structure of Neisserial Surface Protein A (NspA), a Conserved Outer Membrane Protein with Vaccine Potential
journal, April 2003

[18] Genetic Analysis of Agrobacterium
book, January 1991

A Coxiella burnetii phospholipase A homolog pldA is required for optimal growth in macrophages and developmental form lipid remodeling
journal, April 2018

Living on the edge: Simulations of bacterial outer-membrane proteins
journal, July 2016

High-resolution structure of the OmpA membrane domain
journal, April 2000

Identification of the l,d-Transpeptidases Responsible for Attachment of the Braun Lipoprotein to Escherichia coli Peptidoglycan
journal, March 2007

VMD: Visual molecular dynamics
journal, February 1996

The physiology of growth arrest: uniting molecular and environmental microbiology
journal, August 2016

Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations.
journal, January 1981