IM30 IDPs form a membrane-protective carpet upon super-complex disassembly

Abstract

AbstractMembers of the phage shock protein A (PspA) family, including the inner membrane-associated protein of 30 kDa (IM30), are suggested to stabilize stressed cellular membranes. Furthermore, IM30 is essential in thylakoid membrane-containing chloroplasts and cyanobacteria, where it is involved in membrane biogenesis and/or remodeling. While it is well known that PspA and IM30 bind to membranes, the mechanism of membrane stabilization is still enigmatic. Here we report that ring-shaped IM30 super-complexes disassemble on membranes, resulting in formation of a membrane-protecting protein carpet. Upon ring dissociation, the C-terminal domain of IM30 unfolds, and the protomers self-assemble on membranes. IM30 assemblies at membranes have been observed before in vivo and were associated with stress response in cyanobacteria and chloroplasts. These assemblies likely correspond to the here identified carpet structures. Our study defines the thus far enigmatic structural basis for the physiological function of IM30 and related proteins, including PspA, and highlights a hitherto unrecognized concept of membrane stabilization by intrinsically disordered proteins.

Autoren

Benedikt Junglas
Roberto Orru
Amelie Axt
Carmen Siebenaller
Wieland Steinchen
Jennifer Heidrich
Ute A Hellmich
Nadja Hellmann
Eva Wolf
Stefan AL Weber
Dirk Schneider

DOI

10.1038/s42003-020-01314-4

eISSN

2399-3642

Ausgabe der Veröffentlichung

1

Zeitschrift

Communications Biology

Sprache

en

Artikelnummer

595

Online publication date

2020

Status

Published online

Herausgeber

Springer Science and Business Media LLC

Herausgeber URL

http://dx.doi.org/10.1038/s42003-020-01314-4

Datum der Datenerfassung

2022

Titel

IM30 IDPs form a membrane-protective carpet upon super-complex disassembly

Ausgabe der Zeitschrift

3

Data source: Crossref

Abstract

Members of the phage shock protein A (PspA) family, including the inner membrane-associated protein of 30 kDa (IM30), are suggested to stabilize stressed cellular membranes. Furthermore, IM30 is essential in thylakoid membrane-containing chloroplasts and cyanobacteria, where it is involved in membrane biogenesis and/or remodeling. While it is well known that PspA and IM30 bind to membranes, the mechanism of membrane stabilization is still enigmatic. Here we report that ring-shaped IM30 super-complexes disassemble on membranes, resulting in formation of a membrane-protecting protein carpet. Upon ring dissociation, the C-terminal domain of IM30 unfolds, and the protomers self-assemble on membranes. IM30 assemblies at membranes have been observed before in vivo and were associated with stress response in cyanobacteria and chloroplasts. These assemblies likely correspond to the here identified carpet structures. Our study defines the thus far enigmatic structural basis for the physiological function of IM30 and related proteins, including PspA, and highlights a hitherto unrecognized concept of membrane stabilization by intrinsically disordered proteins.

Addresses

Department of Chemistry, Biochemistry, Johannes Gutenberg University Mainz, 55128, Mainz, Germany.

Autoren

Benedikt Junglas
Roberto Orru
Amelie Axt
Carmen Siebenaller
Wieland Steinchen
Jennifer Heidrich
Ute A Hellmich
Nadja Hellmann
Eva Wolf
Stefan AL Weber
Dirk Schneider

DOI

10.1038/s42003-020-01314-4

eISSN

2399-3642

Externe Identifier

PubMed Identifier: 33087858
PubMed Central ID: PMC7577978

Funding acknowledgements

Max Planck Graduate Center at the Max Planck Institutes and the University of Mainz:
NIGMS NIH HHS: P41 GM103311

Open access

true

ISSN

2399-3642

Ausgabe der Veröffentlichung

1

Zeitschrift

Communications biology

Schlüsselwörter

Cell Membrane
Synechocystis
Multiprotein Complexes
Bacterial Proteins
Membrane Proteins
Recombinant Proteins
Liposomes
Microscopy, Atomic Force
Spectrum Analysis
Protein Conformation
Protein Binding
Models, Molecular
Protein Multimerization

Sprache

eng

Medium

Electronic

Online publication date

2020

Open access status

Open Access

Paginierung

595

Datum der Veröffentlichung

2020

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2020

Titel

IM30 IDPs form a membrane-protective carpet upon super-complex disassembly.

Sub types

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

Ausgabe der Zeitschrift

3

Files

https://www.nature.com/articles/s42003-020-01314-4.pdf https://europepmc.org/articles/PMC7577978?pdf=render

Data source: Europe PubMed Central

Abstract

Members of the phage shock protein A (PspA) family, including the inner membrane-associated protein of 30 kDa (IM30), are suggested to stabilize stressed cellular membranes. Furthermore, IM30 is essential in thylakoid membrane-containing chloroplasts and cyanobacteria, where it is involved in membrane biogenesis and/or remodeling. While it is well known that PspA and IM30 bind to membranes, the mechanism of membrane stabilization is still enigmatic. Here we report that ring-shaped IM30 super-complexes disassemble on membranes, resulting in formation of a membrane-protecting protein carpet. Upon ring dissociation, the C-terminal domain of IM30 unfolds, and the protomers self-assemble on membranes. IM30 assemblies at membranes have been observed before in vivo and were associated with stress response in cyanobacteria and chloroplasts. These assemblies likely correspond to the here identified carpet structures. Our study defines the thus far enigmatic structural basis for the physiological function of IM30 and related proteins, including PspA, and highlights a hitherto unrecognized concept of membrane stabilization by intrinsically disordered proteins.

Date of acceptance

2020

Autoren

Benedikt Junglas
Roberto Orru
Amelie Axt
Carmen Siebenaller
Wieland Steinchen
Jennifer Heidrich
Ute A Hellmich
Nadja Hellmann
Eva Wolf
Stefan AL Weber
Dirk Schneider

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/33087858

DOI

10.1038/s42003-020-01314-4

eISSN

2399-3642

Externe Identifier

PubMed Central ID: PMC7577978

Funding acknowledgements

NIGMS NIH HHS: P41 GM103311

Ausgabe der Veröffentlichung

1

Zeitschrift

Commun Biol

Schlüsselwörter

Bacterial Proteins
Cell Membrane
Liposomes
Membrane Proteins
Microscopy, Atomic Force
Models, Molecular
Multiprotein Complexes
Protein Binding
Protein Conformation
Protein Multimerization
Recombinant Proteins
Spectrum Analysis
Synechocystis

Sprache

eng

Country

England

Paginierung

595

PII

10.1038/s42003-020-01314-4

Datum der Veröffentlichung

2020

Status

Published online

Datum, an dem der Datensatz öffentlich gemacht wurde

2021

Titel

IM30 IDPs form a membrane-protective carpet upon super-complex disassembly.

Sub types

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

Ausgabe der Zeitschrift

3

Data source: PubMed

Author's licence

CC-BY

Autoren

Benedikt Junglas
Roberto Orru
Amelie Axt
Carmen Siebenaller
Wieland Steinchen
Jennifer Heidrich
Ute A Hellmich
Nadja Hellmann
Eva Wolf
Stefan AL Weber
Dirk Schneider

Hosting institution

Universitätsbibliothek Mainz

Sammlungen

JGU-Publikationen

Resource version

Published version

DOI

10.1038/s42003-020-01314-4

File(s) embargoed

false

Open access

true

ISSN

2399-3642

Zeitschrift

Communications biology

Schlüsselwörter

540 Chemie
540 Chemistry and allied sciences
570 Biowissenschaften
570 Life sciences

Sprache

eng

Open access status

Open Access

Paginierung

595

Datum der Veröffentlichung

2020

Public URL

https://openscience.ub.uni-mainz.de/handle/20.500.12030/5771

Herausgeber

Springer Nature

Herausgeber URL

https://doi.org/10.1038/s42003-020-01314-4

Datum der Datenerfassung

2021

Datum, an dem der Datensatz öffentlich gemacht wurde

2021

Zugang

Public

Titel

IM30 IDPs form a membrane-protective carpet upon super-complex disassembly

Ausgabe der Zeitschrift

3

Files

x-im30_idps_form-20210420093443760.pdf

Data source: OPENSCIENCE.UB

IM30 IDPs form a membrane-protective carpet upon super-complex disassembly

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