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Cited by 7Bacterial Genetics and BiotechnologyLipid Membrane Structure and BehaviorAntibiotic Resistance in Bacteria

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The AAA+ ATPase RavA and its binding partner ViaA modulate E. coli aminoglycoside sensitivity through interaction with the inner membrane

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Felix, Jan, Bumba, Ladislav, Liesche, Clarissa, Fraudeau, Angélique, Rébeillé, Fabrice, El Khoury, Jessica Y., Huard, Karine, Gallet, Benoit, Moriscot, Christine, Kleman, Jean-Philippe, Duhoo, Yoan, Jessop, Matthew, Kandiah, Eaazhisai, Barras, Frédéric, Jouhet, Juliette, Gutsche, Irina·2022·Nature Communications
DOI 10.1038/s41467-022-32992-9PMC PMC9489729

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Abstract

Enteric bacteria have to adapt to environmental stresses in the human gastrointestinal tract such as acid and nutrient stress, oxygen limitation and exposure to antibiotics. Membrane lipid composition has recently emerged as a key factor for stress adaptation. The E. coli ravA-viaA operon is essential for aminoglycoside bactericidal activity under anaerobiosis but its mechanism of action is unclear. Here we characterise the VWA domain-protein ViaA and its interaction with the AAA+ ATPase RavA, and find that both proteins localise at the inner cell membrane. We demonstrate that RavA and ViaA target specific phospholipids and subsequently identify their lipid-binding sites. We further show that mutations abolishing interaction with lipids restore induced changes in cell membrane morphology and lipid composition. Finally we reveal that these mutations render E. coli gentamicin-resistant under fumarate respiration conditions. Our work thus uncovers a ravA-viaA -based pathway which is mobilised in response to aminoglycosides under anaerobiosis and engaged in cell membrane regulation.

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Metadata

Authors
Felix, J., Bumba, L., Liesche, C., Fraudeau, A., Rébeillé, F., El Khoury, J. Y., Huard, K., Gallet, B., Moriscot, C., Kleman, J.-P., Duhoo, Y., Jessop, M., Kandiah, E., Barras, F., Jouhet, J., & Gutsche, I.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Gutsche, Irina
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-09-20
Volume
13
Issue
1
Pages
5502-5502
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-022-32992-9
PMC
PMC9489729
OpenAlex
W4296774165
Cited by
7
References
5
Citations by year
2026: 1 · 2025: 1 · 2024: 1 · 2023: 4
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Infrastructures en Biologie Santé et Agronomie (ANR-17-EURE-0003)
  • European Commission (ANR-17-EURE-0003, LX22NPO5103, UAR 3518 CNRS-CEA-UGA-EMBL, 789385, 647784, HORIZON2020)
  • Agence Nationale de la Recherche (ANR-10-INSB-05-01., UAR 3518 CNRS-CEA-UGA-EMBL, ANR-17-EURE-0003, 10-INSB-05-01, ANR- 10-INSB-05, ANR-17-EURE-, ANR-17, ANR-10, ANR-10-INBS-0005, ANR-10-LABX-0049)
  • Ministerstvo Školství, Mládeže a Tělovýchovy (LM2018133)
  • Centre National de la Recherche Scientifique (ANR‐17‐EURE‐0003, UAR 3518 CNRS-CEA-UGA-EMBL)
  • French Infrastructure for Integrated Structural Biology (UAR 3518 CNRS-CEA-UGA-EMBL, ANR-17-EURE-0003, ANR-10-INBS-0005, ANR-10- INSB-05, ANR-10-INSB-0501, ANR-10-INBS-000502, INSB-05, ANR-10-INBS)
  • Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
  • H2020 Marie Skłodowska-Curie Actions (ANR-17-EURE-0003, HORIZON2020)
  • NextGenerationEU
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
Keywords
Rava, AAA+ ATPase, VWA domain, gentamicin resistance, Escherichia coli, inner membrane, membrane lipid composition, lipid binding sites, membrane morphology, anaerobic stress, fumarate respiration, stress adaptation
MeSH terms
ATPases Associated with Diverse Cellular Activities, Adenosine Triphosphatases, Aminoglycosides, Anti-Bacterial Agents, Escherichia coli, Fumarates, Gentamicins, Membrane Lipids, Oxygen, Phospholipids, Escherichia coli Proteins

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