The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins

Kamel El Omari, Sai Li, Abhay Kotecha, Thomas S. Walter, Eduardo Bignon, Karl Harlos, Pentti Somerharju, Felix de Haas, Daniel Clare, Mika Molin, Felipe Hurtado, Mengqiu Li, Jonathan M. Grimes, Dennis Henry Bamford, Nicole D. Tischler, Juha T. Huiskonen, David I. Stuart, Elina Roine

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Lipid membrane fusion is an essential function in many biological processes. Detailed mechanisms of membrane fusion and the protein structures involved have been mainly studied in eukaryotic systems, whereas very little is known about membrane fusion in prokaryotes. Haloarchaeal pleomorphic viruses (HRPVs) have a membrane envelope decorated with spikes that are presumed to be responsible for host attachment and membrane fusion. Here we determine atomic structures of the ectodomains of the 57-kDa spike protein VP5 from two related HRPVs revealing a previously unreported V-shaped fold. By Volta phase
plate cryo-electron tomography we show that VP5 is monomeric on the viral surface, and we establish the orientation of the molecules with respect to the viral membrane. We also show that the viral membrane fuses with the host cytoplasmic membrane in a process mediated by VP5. This sheds light on protein structures involved in prokaryotic membrane fusion.
Original languageEnglish
Article number846
JournalNature Communications
Volume10
Number of pages11
ISSN2041-1723
DOIs
Publication statusPublished - 19 Feb 2019
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 1183 Plant biology, microbiology, virology
  • Archaea
  • Virus
  • Prokaryote
  • 1182 Biochemistry, cell and molecular biology
  • Cryo-ET
  • X-ray crystal structure
  • Membrane fusion
  • Fusion proteins
  • NANOLITRE CRYSTALLIZATION EXPERIMENTS
  • INFLUENZA-VIRUS
  • SYSTEM
  • VISUALIZATION

Cite this

El Omari, Kamel ; Li, Sai ; Kotecha, Abhay ; Walter, Thomas S. ; Bignon, Eduardo ; Harlos, Karl ; Somerharju, Pentti ; Haas, Felix de ; Clare, Daniel ; Molin, Mika ; Hurtado, Felipe ; Li, Mengqiu ; Grimes, Jonathan M. ; Bamford, Dennis Henry ; Tischler, Nicole D. ; Huiskonen, Juha T. ; Stuart, David I. ; Roine, Elina. / The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins. In: Nature Communications. 2019 ; Vol. 10.
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title = "The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins",
abstract = "Lipid membrane fusion is an essential function in many biological processes. Detailed mechanisms of membrane fusion and the protein structures involved have been mainly studied in eukaryotic systems, whereas very little is known about membrane fusion in prokaryotes. Haloarchaeal pleomorphic viruses (HRPVs) have a membrane envelope decorated with spikes that are presumed to be responsible for host attachment and membrane fusion. Here we determine atomic structures of the ectodomains of the 57-kDa spike protein VP5 from two related HRPVs revealing a previously unreported V-shaped fold. By Volta phaseplate cryo-electron tomography we show that VP5 is monomeric on the viral surface, and we establish the orientation of the molecules with respect to the viral membrane. We also show that the viral membrane fuses with the host cytoplasmic membrane in a process mediated by VP5. This sheds light on protein structures involved in prokaryotic membrane fusion.",
keywords = "1183 Plant biology, microbiology, virology, Archaea, Virus, Prokaryote, 1182 Biochemistry, cell and molecular biology, Cryo-ET, X-ray crystal structure, Membrane fusion, Fusion proteins, NANOLITRE CRYSTALLIZATION EXPERIMENTS, INFLUENZA-VIRUS, SYSTEM, VISUALIZATION",
author = "{El Omari}, Kamel and Sai Li and Abhay Kotecha and Walter, {Thomas S.} and Eduardo Bignon and Karl Harlos and Pentti Somerharju and Haas, {Felix de} and Daniel Clare and Mika Molin and Felipe Hurtado and Mengqiu Li and Grimes, {Jonathan M.} and Bamford, {Dennis Henry} and Tischler, {Nicole D.} and Huiskonen, {Juha T.} and Stuart, {David I.} and Elina Roine",
year = "2019",
month = "2",
day = "19",
doi = "10.1038/s41467-019-08728-7",
language = "English",
volume = "10",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",

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El Omari, K, Li, S, Kotecha, A, Walter, TS, Bignon, E, Harlos, K, Somerharju, P, Haas, FD, Clare, D, Molin, M, Hurtado, F, Li, M, Grimes, JM, Bamford, DH, Tischler, ND, Huiskonen, JT, Stuart, DI & Roine, E 2019, 'The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins', Nature Communications, vol. 10, 846. https://doi.org/10.1038/s41467-019-08728-7

The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins. / El Omari, Kamel; Li, Sai; Kotecha, Abhay; Walter, Thomas S.; Bignon, Eduardo; Harlos, Karl; Somerharju, Pentti; Haas, Felix de; Clare, Daniel; Molin, Mika; Hurtado, Felipe; Li, Mengqiu; Grimes, Jonathan M.; Bamford, Dennis Henry; Tischler, Nicole D.; Huiskonen, Juha T.; Stuart, David I.; Roine, Elina.

In: Nature Communications, Vol. 10, 846, 19.02.2019.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - The structure of a prokaryotic viral envelope protein expands the landscape of membrane fusion proteins

AU - El Omari, Kamel

AU - Li, Sai

AU - Kotecha, Abhay

AU - Walter, Thomas S.

AU - Bignon, Eduardo

AU - Harlos, Karl

AU - Somerharju, Pentti

AU - Haas, Felix de

AU - Clare, Daniel

AU - Molin, Mika

AU - Hurtado, Felipe

AU - Li, Mengqiu

AU - Grimes, Jonathan M.

AU - Bamford, Dennis Henry

AU - Tischler, Nicole D.

AU - Huiskonen, Juha T.

AU - Stuart, David I.

AU - Roine, Elina

PY - 2019/2/19

Y1 - 2019/2/19

N2 - Lipid membrane fusion is an essential function in many biological processes. Detailed mechanisms of membrane fusion and the protein structures involved have been mainly studied in eukaryotic systems, whereas very little is known about membrane fusion in prokaryotes. Haloarchaeal pleomorphic viruses (HRPVs) have a membrane envelope decorated with spikes that are presumed to be responsible for host attachment and membrane fusion. Here we determine atomic structures of the ectodomains of the 57-kDa spike protein VP5 from two related HRPVs revealing a previously unreported V-shaped fold. By Volta phaseplate cryo-electron tomography we show that VP5 is monomeric on the viral surface, and we establish the orientation of the molecules with respect to the viral membrane. We also show that the viral membrane fuses with the host cytoplasmic membrane in a process mediated by VP5. This sheds light on protein structures involved in prokaryotic membrane fusion.

AB - Lipid membrane fusion is an essential function in many biological processes. Detailed mechanisms of membrane fusion and the protein structures involved have been mainly studied in eukaryotic systems, whereas very little is known about membrane fusion in prokaryotes. Haloarchaeal pleomorphic viruses (HRPVs) have a membrane envelope decorated with spikes that are presumed to be responsible for host attachment and membrane fusion. Here we determine atomic structures of the ectodomains of the 57-kDa spike protein VP5 from two related HRPVs revealing a previously unreported V-shaped fold. By Volta phaseplate cryo-electron tomography we show that VP5 is monomeric on the viral surface, and we establish the orientation of the molecules with respect to the viral membrane. We also show that the viral membrane fuses with the host cytoplasmic membrane in a process mediated by VP5. This sheds light on protein structures involved in prokaryotic membrane fusion.

KW - 1183 Plant biology, microbiology, virology

KW - Archaea

KW - Virus

KW - Prokaryote

KW - 1182 Biochemistry, cell and molecular biology

KW - Cryo-ET

KW - X-ray crystal structure

KW - Membrane fusion

KW - Fusion proteins

KW - NANOLITRE CRYSTALLIZATION EXPERIMENTS

KW - INFLUENZA-VIRUS

KW - SYSTEM

KW - VISUALIZATION

U2 - 10.1038/s41467-019-08728-7

DO - 10.1038/s41467-019-08728-7

M3 - Article

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 846

ER -