The SARS-CoV-2 nucleocapsid phosphoprotein forms mutually exclusive condensates with RNA and the membrane-associated M protein

Nat Commun. 2021 Jan 21;12(1):502. doi: 10.1038/s41467-020-20768-y.

Abstract

The multifunctional nucleocapsid (N) protein in SARS-CoV-2 binds the ~30 kb viral RNA genome to aid its packaging into the 80-90 nm membrane-enveloped virion. The N protein is composed of N-terminal RNA-binding and C-terminal dimerization domains that are flanked by three intrinsically disordered regions. Here we demonstrate that the N protein's central disordered domain drives phase separation with RNA, and that phosphorylation of an adjacent serine/arginine rich region modulates the physical properties of the resulting condensates. In cells, N forms condensates that recruit the stress granule protein G3BP1, highlighting a potential role for N in G3BP1 sequestration and stress granule inhibition. The SARS-CoV-2 membrane (M) protein independently induces N protein phase separation, and three-component mixtures of N + M + RNA form condensates with mutually exclusive compartments containing N + M or N + RNA, including annular structures in which the M protein coats the outside of an N + RNA condensate. These findings support a model in which phase separation of the SARS-CoV-2 N protein contributes both to suppression of the G3BP1-dependent host immune response and to packaging genomic RNA during virion assembly.

Publication types

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

MeSH terms

  • COVID-19 / genetics
  • COVID-19 / metabolism
  • COVID-19 / virology*
  • Cell Membrane / virology
  • Coronavirus Nucleocapsid Proteins / chemistry
  • Coronavirus Nucleocapsid Proteins / genetics
  • Coronavirus Nucleocapsid Proteins / metabolism*
  • DNA Helicases / genetics
  • DNA Helicases / metabolism
  • Humans
  • Phosphoproteins / chemistry
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Poly-ADP-Ribose Binding Proteins / genetics
  • Poly-ADP-Ribose Binding Proteins / metabolism
  • Protein Binding
  • Protein Domains
  • RNA Helicases / genetics
  • RNA Helicases / metabolism
  • RNA Recognition Motif Proteins / genetics
  • RNA Recognition Motif Proteins / metabolism
  • RNA, Viral / genetics
  • RNA, Viral / metabolism*
  • SARS-CoV-2 / chemistry
  • SARS-CoV-2 / genetics
  • SARS-CoV-2 / metabolism*
  • Viral Matrix Proteins / chemistry
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / metabolism*

Substances

  • Coronavirus Nucleocapsid Proteins
  • Phosphoproteins
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • RNA, Viral
  • Viral Matrix Proteins
  • membrane protein, SARS-CoV-2
  • nucleocapsid phosphoprotein, SARS-CoV-2
  • DNA Helicases
  • G3BP1 protein, human
  • RNA Helicases