Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation

Nat Struct Mol Biol. 2020 Mar;27(3):281-287. doi: 10.1038/s41594-020-0387-7. Epub 2020 Mar 2.

Abstract

Carboxysomes are bacterial microcompartments that function as the centerpiece of the bacterial CO2-concentrating mechanism by facilitating high CO2 concentrations near the carboxylase Rubisco. The carboxysome self-assembles from thousands of individual proteins into icosahedral-like particles with a dense enzyme cargo encapsulated within a proteinaceous shell. In the case of the α-carboxysome, there is little molecular insight into protein-protein interactions that drive the assembly process. Here, studies on the α-carboxysome from Halothiobacillus neapolitanus demonstrate that Rubisco interacts with the N terminus of CsoS2, a multivalent, intrinsically disordered protein. X-ray structural analysis of the CsoS2 interaction motif bound to Rubisco reveals a series of conserved electrostatic interactions that are only made with properly assembled hexadecameric Rubisco. Although biophysical measurements indicate that this single interaction is weak, its implicit multivalency induces high-affinity binding through avidity. Taken together, our results indicate that CsoS2 acts as an interaction hub to condense Rubisco and enable efficient α-carboxysome formation.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Carbon Cycle / physiology
  • Cloning, Molecular
  • Crystallography, X-Ray
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression
  • Genetic Vectors / chemistry
  • Genetic Vectors / metabolism
  • Halothiobacillus / chemistry*
  • Halothiobacillus / genetics
  • Halothiobacillus / metabolism
  • Intrinsically Disordered Proteins / chemistry*
  • Intrinsically Disordered Proteins / genetics
  • Intrinsically Disordered Proteins / metabolism
  • Models, Molecular
  • Organelles / chemistry*
  • Organelles / metabolism
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Ribulose-Bisphosphate Carboxylase / chemistry*
  • Ribulose-Bisphosphate Carboxylase / genetics
  • Ribulose-Bisphosphate Carboxylase / metabolism
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Static Electricity

Substances

  • Bacterial Proteins
  • Intrinsically Disordered Proteins
  • Recombinant Proteins
  • Ribulose-Bisphosphate Carboxylase