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PreprintCited by 20Bacterial Genetics and BiotechnologyEscherichia coli research studiesAdvanced Electron Microscopy Techniques and Applications

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LptM promotes oxidative maturation of the lipopolysaccharide translocon by substrate binding mimicry

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Yang, Yiying, Chen, Haoxiang, Corey, Robin A., Morales, Violette, Quentin, Yves, Froment, Carine, Caumont-Sarcos, Anne, Albenne, Cécile, Burlet-Schiltz, Odile, Ranava, David, Stansfeld, Phillip J., Marcoux, Julien, Ieva, Raffaele·2023·Nature Communications
DOI 10.1101/2023.01.02.522452PMC PMC10567701

Preprint — published as 10.1038/s41467-023-42007-w · Paper page

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Abstract

Insertion of lipopolysaccharide (LPS) into the outer membrane (OM) of Gram-negative bacteria is mediated by a druggable OM translocon consisting of a β-barrel membrane protein, LptD, and a lipoprotein, LptE. The β-barrel assembly machinery (BAM) assembles LptD together with LptE to form a plug-and-barrel structure. In the enterobacterium Escherichia coli , formation of two native disulfide bonds in LptD controls LPS translocon activation. Here we report the discovery of LptM (formerly YifL), a conserved lipoprotein that assembles together with LptD and LptE at the BAM complex. We demonstrate that LptM stabilizes a conformation of LptD that can efficiently acquire native disulfide bonds and be released as mature LPS translocon by the BAM complex. Inactivation of LptM causes the accumulation of non-natively oxidized LptD, making disulfide bond isomerization by DsbC become essential for viability. Our structural prediction and biochemical analyses indicate that LptM binds to sites in both LptD and LptE that are proposed to coordinate LPS insertion into the OM. These results suggest that LptM facilitates oxidative maturation of LptD by mimicking LPS binding, thereby activating the LPS translocon.

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Metadata

Authors
Yang, Y., Chen, H., Corey, R. A., Morales, V., Quentin, Y., Froment, C., Caumont-Sarcos, A., Albenne, C., Burlet-Schiltz, O., Ranava, D., Stansfeld, P. J., Marcoux, J., & Ieva, R.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University of Bristol (GB)
  • University of Warwick (GB)
Corresponding author
Ieva, Raffaele
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2023-01-03
Volume
14
Issue
1
Pages
6368-6368
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2023.01.02.522452
PMC
PMC10567701
OpenAlex
W4387540011
Cited by
20
References
1
Citations by year
2026: 6 · 2025: 11 · 2024: 3
FWCI
3.32
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Explore Bristol Research (publishedVersion, other-oa)
  • Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
  • HAL (submittedVersion)
  • HAL (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Bristol Research (University of Bristol) (submittedVersion, other-oa)
Funders
  • Wellcome Trust
  • University of Warwick (EP/T022108/1)
  • Agence Nationale de la Recherche (ANR-10-INBS-0008, ANR-10-INBS-08, Proteomics French Infrastructure,ANR-10-INBS-08, ANR-10)
  • Keio University
  • China Scholarship Council
  • Centre National de la Recherche Scientifique
  • Engineering and Physical Sciences Research Council (EP/P020232/1, EP/R029407/1, EP/T022108/1, R029407, P020232, P020232/1, EP/P020232)
  • Biotechnology and Biological Sciences Research Council (BB/R002517/1, BB/S003339/1, BB/P01948X/1, P01948X, R002517, S003339, BB/P01948X/2)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
Keywords
LptD, outer membrane biogenesis, β-barrel assembly machinery, disulfide bond formation, DsbC, Escherichia coli, Enterobacteriaceae
MeSH terms
Bacterial Outer Membrane Proteins, Cell Membrane, Disulfides, Escherichia coli, Lipopolysaccharides, Lipoproteins, Oxidative Stress, Escherichia coli Proteins

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