Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Jiwei Liu; Matteo Tassinari; Diorge Souza; Souvik Naskar; Jeffrey K. Noel; Olga Bohuszewicz; Martin Buck; Tom Williams; Buzz Baum; Harry H. Low

doi:10.1016/j.cell.2021.05.041

Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Jiwei Liu
, Matteo Tassinari
, Diorge Souza
, Souvik Naskar
, Jeffrey K. Noel
, Olga Bohuszewicz
, Martin Buck
, Tom Williams
, Buzz Baum
, Harry H. Low

Department of Life Sciences

University of Oxford
Imperial College London
University College London
Max Delbrück Center for Molecular Medicine

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

83 Citations (SciVal)

Abstract

Membrane remodeling and repair are essential for all cells. Proteins that perform these functions include Vipp1/IM30 in photosynthetic plastids, PspA in bacteria, and ESCRT-III in eukaryotes. Here, using a combination of evolutionary and structural analyses, we show that these protein families are homologous and share a common ancient evolutionary origin that likely predates the last universal common ancestor. This homology is evident in cryo-electron microscopy structures of Vipp1 rings from the cyanobacterium Nostoc punctiforme presented over a range of symmetries. Each ring is assembled from rungs that stack and progressively tilt to form dome-shaped curvature. Assembly is facilitated by hinges in the Vipp1 monomer, similar to those in ESCRT-III proteins, which allow the formation of flexible polymers. Rings have an inner lumen that is able to bind and deform membranes. Collectively, these data suggest conserved mechanistic principles that underlie Vipp1, PspA, and ESCRT-III-dependent membrane remodeling across all domains of life.

Original language	English
Journal	Cell
Volume	184
Issue number	15
Early online date	23 Jun 2021
DOIs	https://doi.org/10.1016/j.cell.2021.05.041
Publication status	Published - 8 Jul 2021

Data Availability Statement

3D cryo-EM density maps produced in this study have been deposited in the Electron Microscopy Data Bank with accession code EMD-11468, EMD-11469, EMD-11470, EMD-11478, EMD-11481, EMD-11482 and EMD-11483 for Vipp1C11-C17, respectively. Atomic coordinates have been deposited in the Protein Data Bank (PDB) under accession code 6ZVR, 6ZVS, 6ZVT, 6ZW4, 6ZW5, 6ZW6 and 6ZW7 for Vipp1C11-C17, respectively.

Acknowledgements

We thank Diamond for access and support of the cryo-EM facilities at the UK National Electron Bio-Imaging Centre (eBIC) funded by the Wellcome Trust, MRC, and BBSRC. We thank Paul Simpson for in-house EM support. We thank Jan Löwe for acting as collaboration catalyst. We thank BBSRC for a doctoral training program PhD to O.B. T.A.W. is supported by a Royal Society University Research Fellowship (UF140626).

Funding

This work was funded by a Wellcome Trust Senior Research Fellowship (215553/Z/19/Z) and previously by a Wellcome Trust Career Development Fellowship (200074/Z/15/Z) to H.H.L. This work was also funded by Wellcome Trust funding to B.B., which supported D.P.S. (203276/Z/16/Z), and via MRC support for the Baum team.

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title = "Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily",

abstract = "Membrane remodeling and repair are essential for all cells. Proteins that perform these functions include Vipp1/IM30 in photosynthetic plastids, PspA in bacteria, and ESCRT-III in eukaryotes. Here, using a combination of evolutionary and structural analyses, we show that these protein families are homologous and share a common ancient evolutionary origin that likely predates the last universal common ancestor. This homology is evident in cryo-electron microscopy structures of Vipp1 rings from the cyanobacterium Nostoc punctiforme presented over a range of symmetries. Each ring is assembled from rungs that stack and progressively tilt to form dome-shaped curvature. Assembly is facilitated by hinges in the Vipp1 monomer, similar to those in ESCRT-III proteins, which allow the formation of flexible polymers. Rings have an inner lumen that is able to bind and deform membranes. Collectively, these data suggest conserved mechanistic principles that underlie Vipp1, PspA, and ESCRT-III-dependent membrane remodeling across all domains of life.",

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AU - Tassinari, Matteo

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AU - Naskar, Souvik

AU - Noel, Jeffrey K.

AU - Bohuszewicz, Olga

AU - Buck, Martin

AU - Williams, Tom

AU - Baum, Buzz

AU - Low, Harry H.

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Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Abstract

Data Availability Statement

Acknowledgements

Funding

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