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^*

^*Corresponding author for this work

School of Biological Sciences

Research output: Contribution to journal › Article (Academic Journal) › peer-review

3 Citations (Scopus)

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
Pages (from-to)	3660-3673.e18
Number of pages	33
Journal	Cell
Volume	184
Issue number	14
DOIs	https://doi.org/10.1016/j.cell.2021.05.041
Publication status	Published - 23 Jun 2021

Bibliographical note

Funding Information:
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 ). 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.

Publisher Copyright:
© 2021 The Authors

Access to Document

10.1016/j.cell.2021.05.041

Full-text PDF (Publisher's VOR)
This is the final published version of the article (version of record). It first appeared online via Cell at 10.1016/j.cell.2021.05.041. Please refer to any applicable terms of use of the publisher.
Final published version, 13 MBLicence: CC BY

Cite this

@article{d661406566d941e6bf00566e79ffd5dc,

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.",

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

note = "Funding Information: 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 L{\"o}we 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 ). 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. Publisher Copyright: {\textcopyright} 2021 The Authors",

year = "2021",

month = jun,

day = "23",

doi = "10.1016/j.cell.2021.05.041",

language = "English",

volume = "184",

pages = "3660--3673.e18",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "14",

}

Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. / Liu, Jiwei; Tassinari, Matteo; Souza, Diorge; Naskar, Souvik; Noel, Jeffrey K.; Bohuszewicz, Olga; Buck, Martin; Williams, Tom; Baum, Buzz; Low, Harry H.

In: Cell, Vol. 184, No. 14, 23.06.2021, p. 3660-3673.e18.

Research output: Contribution to journal › Article (Academic Journal) › peer-review

TY - JOUR

T1 - Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

AU - Liu, Jiwei

AU - Tassinari, Matteo

AU - Souza, Diorge

AU - Naskar, Souvik

AU - Noel, Jeffrey K.

AU - Bohuszewicz, Olga

AU - Buck, Martin

AU - Williams, Tom

AU - Baum, Buzz

AU - Low, Harry H.

N1 - Funding Information: 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 ). 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. Publisher Copyright: © 2021 The Authors

PY - 2021/6/23

Y1 - 2021/6/23

N2 - 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.

AB - 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.

U2 - 10.1016/j.cell.2021.05.041

DO - 10.1016/j.cell.2021.05.041

M3 - Article (Academic Journal)

VL - 184

SP - 3660-3673.e18

JO - Cell

JF - Cell

SN - 0092-8674

IS - 14

ER -

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

Abstract

Bibliographical note

Access to Document

Fingerprint

Cite this