Posttranslational insertion of small membrane proteins by the bacterial signal recognition particle.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
09 2020
Historique:
received: 05 05 2020
accepted: 02 09 2020
revised: 12 10 2020
pubmed: 1 10 2020
medline: 15 12 2020
entrez: 30 9 2020
Statut: epublish

Résumé

Small membrane proteins represent a largely unexplored yet abundant class of proteins in pro- and eukaryotes. They essentially consist of a single transmembrane domain and are associated with stress response mechanisms in bacteria. How these proteins are inserted into the bacterial membrane is unknown. Our study revealed that in Escherichia coli, the 27-amino-acid-long model protein YohP is recognized by the signal recognition particle (SRP), as indicated by in vivo and in vitro site-directed cross-linking. Cross-links to SRP were also observed for a second small membrane protein, the 33-amino-acid-long YkgR. However, in contrast to the canonical cotranslational recognition by SRP, SRP was found to bind to YohP posttranslationally. In vitro protein transport assays in the presence of a SecY inhibitor and proteoliposome studies demonstrated that SRP and its receptor FtsY are essential for the posttranslational membrane insertion of YohP by either the SecYEG translocon or by the YidC insertase. Furthermore, our data showed that the yohP mRNA localized preferentially and translation-independently to the bacterial membrane in vivo. In summary, our data revealed that YohP engages an unique SRP-dependent posttranslational insertion pathway that is likely preceded by an mRNA targeting step. This further highlights the enormous plasticity of bacterial protein transport machineries.

Identifiants

pubmed: 32997663
doi: 10.1371/journal.pbio.3000874
pii: PBIOLOGY-D-20-01278
pmc: PMC7549839
doi:

Substances chimiques

Escherichia coli Proteins 0
Membrane Proteins 0
RNA, Messenger 0
SEC Translocation Channels 0
Signal Recognition Particle 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000874

Subventions

Organisme : Wellcome Trust
ID : 204957/Z/16/Z
Pays : United Kingdom
Organisme : European Research Council
ID : 769065
Pays : International
Organisme : NIGMS NIH HHS
ID : R15 GM116032
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Ruth Steinberg (R)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Andrea Origi (A)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Ana Natriashvili (A)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Pinku Sarmah (P)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Mariya Licheva (M)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Princess M Walker (PM)

Department of Chemistry, Ball State University, Muncie, Indiana, United States of America.

Claudine Kraft (C)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Stephen High (S)

School of Biological Sciences, University of Manchester, Manchester, United Kingdom.

Joen Luirink (J)

Molecular Microbiology, AIMMS, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Wei Q Shi (WQ)

Department of Chemistry, Ball State University, Muncie, Indiana, United States of America.

Martin Helmstädter (M)

Internal Medicine IV, Department of Medicine, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Maximilian H Ulbrich (MH)

Internal Medicine IV, Department of Medicine, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
BIOSS Centre for Biological Signalling Studies, University of Freiburg, Freiburg, Germany.

Hans-Georg Koch (HG)

Institute of Biochemistry and Molecular Biology, ZBMZ, Faculty of Medicine, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

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Classifications MeSH