Asgard archaea reveal the conserved principles of ESCRT-III membrane remodeling

Diorge P. Souza; Javier Espadas; Sami Chaaban; Edmund R. R. Moody; Tomoyuki Hatano; Mohan Balasubramanian; Tom A. Williams; Aurélien Roux; Buzz Baum

doi:10.1126/sciadv.ads5255

Asgard archaea reveal the conserved principles of ESCRT-III membrane remodeling

Diorge P. Souza
, Javier Espadas
, Sami Chaaban
, Edmund R. R. Moody
, Tomoyuki Hatano
, Mohan Balasubramanian
, Tom A. Williams
, Aurélien Roux
, Buzz Baum

MRC Laboratory of Molecular Biology
University of Geneva
University of Bristol
University of Warwick

Research output: Contribution to journal › Article › peer-review

10 Citations (SciVal)

Abstract

ESCRT-III proteins assemble into composite polymers that undergo stepwise changes in composition and structure to deform membranes across the tree of life. Here, using a phylogenetic analysis, we demonstrate that the two endosomal sorting complex required for transport III (ESCRT-III) proteins present in eukaryote’s closest Asgard archaeal relatives are evolutionarily related to the B- and A-type eukaryotic paralogs that initiate and execute membrane remodeling, respectively. We show that Asgard ESCRT-IIIB assembles into parallel arrays on planar membranes to initiate membrane deformation, from where it recruits ESCRT-IIIA to generate composite polymers. Last, we show that Asgard ESCRT-IIIA is able to remodel membranes into tubes as a likely prelude to scission. Together, these data reveal a set of conserved principles governing ESCRT-III–dependent membrane remodeling that first emerged in a two-component ESCRT-III system in archaea.

Original language	English
Article number	eads5255
Journal	Science Advances
Volume	11
Issue number	6
DOIs	https://doi.org/10.1126/sciadv.ads5255
Publication status	Published - 7 Feb 2025

Bibliographical note

Publisher Copyright:
Copyright © 2025 The Authors, some rights reserved.

Data Availability Statement

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Atomic coordinates and cryo-EM maps have been deposited in the Protein Data Bank/Electron Microscopy Data Bank under accession codes 9FTL/50748 (off-membrane filament) and 9FTM/50749 (on-membrane array).

Funding

We would like to thank the staff of the MRC LMB and DCI Geneva EM facilities, J. L\u00F6we, and S. Scheres for support on EM sample preparation, data collection, and cryo-EM image processing. We would also like to thank F. Humbert and R. Ferreira in the Roux lab for technical support on protein expression and purification, A. P. Carter for discussions and suggestions, and J. Grimmet and the Scientific Computing team at the MRC LMB for providing computing resources. We would like to thank the following people for the feedback on the manuscript: K. Kuo, J. L\u00F6we, A. Prada, A. Saric, and J. Tran. This work was supported by Wellcome Trust grant 203276/Z/16/Z (to B.B. and D.P.S.), UK Medical Research Council grant MC_UP_1201/27 (to B.B.), EMBO long-term fellowship ALTF 989-2022 (to J.E.), Swiss National Fund for Research grant CRSII5_189996 (to A.R.), Swiss National Fund for Research grant 310030_200793 (to A.R.), European Research Council Synergy grant 951324-R2-TENSION (to A.R.), Wellcome Trust grant 210711/Z/18/Z (to A. P. Carter and S.C.), Wellcome Trust collaborative award 203276/Z/16/Z (to M.B. and B.B.), and Gordon and Betty Moore Foundation grant GBMF9741 (to T.W. and E.M.).

Funders	Funder number
Medical Research Council	MC_UP_1201/27
European Molecular Biology Organization	ALTF 989-2022
The Wellcome Trust	203276/Z/16/Z
European Research Council	210711/Z/18/Z, 951324-R2-TENSION
Gordon and Betty Moore Foundation	GBMF9741
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	CRSII5_189996, 310030_200793

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title = "Asgard archaea reveal the conserved principles of ESCRT-III membrane remodeling",

abstract = "ESCRT-III proteins assemble into composite polymers that undergo stepwise changes in composition and structure to deform membranes across the tree of life. Here, using a phylogenetic analysis, we demonstrate that the two endosomal sorting complex required for transport III (ESCRT-III) proteins present in eukaryote{\textquoteright}s closest Asgard archaeal relatives are evolutionarily related to the B- and A-type eukaryotic paralogs that initiate and execute membrane remodeling, respectively. We show that Asgard ESCRT-IIIB assembles into parallel arrays on planar membranes to initiate membrane deformation, from where it recruits ESCRT-IIIA to generate composite polymers. Last, we show that Asgard ESCRT-IIIA is able to remodel membranes into tubes as a likely prelude to scission. Together, these data reveal a set of conserved principles governing ESCRT-III–dependent membrane remodeling that first emerged in a two-component ESCRT-III system in archaea.",

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AU - Souza, Diorge P.

AU - Espadas, Javier

AU - Chaaban, Sami

AU - Moody, Edmund R. R.

AU - Hatano, Tomoyuki

AU - Balasubramanian, Mohan

AU - Williams, Tom A.

AU - Roux, Aurélien

AU - Baum, Buzz

PY - 2025/2/7

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N2 - ESCRT-III proteins assemble into composite polymers that undergo stepwise changes in composition and structure to deform membranes across the tree of life. Here, using a phylogenetic analysis, we demonstrate that the two endosomal sorting complex required for transport III (ESCRT-III) proteins present in eukaryote’s closest Asgard archaeal relatives are evolutionarily related to the B- and A-type eukaryotic paralogs that initiate and execute membrane remodeling, respectively. We show that Asgard ESCRT-IIIB assembles into parallel arrays on planar membranes to initiate membrane deformation, from where it recruits ESCRT-IIIA to generate composite polymers. Last, we show that Asgard ESCRT-IIIA is able to remodel membranes into tubes as a likely prelude to scission. Together, these data reveal a set of conserved principles governing ESCRT-III–dependent membrane remodeling that first emerged in a two-component ESCRT-III system in archaea.

AB - ESCRT-III proteins assemble into composite polymers that undergo stepwise changes in composition and structure to deform membranes across the tree of life. Here, using a phylogenetic analysis, we demonstrate that the two endosomal sorting complex required for transport III (ESCRT-III) proteins present in eukaryote’s closest Asgard archaeal relatives are evolutionarily related to the B- and A-type eukaryotic paralogs that initiate and execute membrane remodeling, respectively. We show that Asgard ESCRT-IIIB assembles into parallel arrays on planar membranes to initiate membrane deformation, from where it recruits ESCRT-IIIA to generate composite polymers. Last, we show that Asgard ESCRT-IIIA is able to remodel membranes into tubes as a likely prelude to scission. Together, these data reveal a set of conserved principles governing ESCRT-III–dependent membrane remodeling that first emerged in a two-component ESCRT-III system in archaea.

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Asgard archaea reveal the conserved principles of ESCRT-III membrane remodeling

Abstract

Bibliographical note

Data Availability Statement

Funding

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