Molecular insights into capsular polysaccharide secretion

Nature. 2024 Apr;628(8009):901-909. doi: 10.1038/s41586-024-07248-9. Epub 2024 Apr 3.

Abstract

Capsular polysaccharides (CPSs) fortify the cell boundaries of many commensal and pathogenic bacteria1. Through the ABC-transporter-dependent biosynthesis pathway, CPSs are synthesized intracellularly on a lipid anchor and secreted across the cell envelope by the KpsMT ABC transporter associated with the KpsE and KpsD subunits1,2. Here we use structural and functional studies to uncover crucial steps of CPS secretion in Gram-negative bacteria. We show that KpsMT has broad substrate specificity and is sufficient for the translocation of CPSs across the inner bacterial membrane, and we determine the cell surface organization and localization of CPSs using super-resolution fluorescence microscopy. Cryo-electron microscopy analyses of the KpsMT-KpsE complex in six different states reveal a KpsE-encaged ABC transporter, rigid-body conformational rearrangements of KpsMT during ATP hydrolysis and recognition of a glycolipid inside a membrane-exposed electropositive canyon. In vivo CPS secretion assays underscore the functional importance of canyon-lining basic residues. Combined, our analyses suggest a molecular model of CPS secretion by ABC transporters.

Publication types

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

MeSH terms

  • ATP-Binding Cassette Transporters / chemistry
  • ATP-Binding Cassette Transporters / metabolism
  • ATP-Binding Cassette Transporters / ultrastructure
  • Adenosine Triphosphate / metabolism
  • Bacterial Capsules* / chemistry
  • Bacterial Capsules* / metabolism
  • Bacterial Capsules* / ultrastructure
  • Cell Membrane / chemistry
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Cryoelectron Microscopy
  • Escherichia coli Proteins* / chemistry
  • Escherichia coli Proteins* / metabolism
  • Escherichia coli Proteins* / ultrastructure
  • Escherichia coli* / chemistry
  • Escherichia coli* / metabolism
  • Escherichia coli* / ultrastructure
  • Glycolipids / chemistry
  • Glycolipids / metabolism
  • Hydrolysis
  • Microscopy, Fluorescence
  • Models, Molecular
  • Polysaccharides, Bacterial* / chemistry
  • Polysaccharides, Bacterial* / metabolism
  • Substrate Specificity

Substances

  • Adenosine Triphosphate
  • ATP-Binding Cassette Transporters
  • Escherichia coli Proteins
  • Glycolipids
  • KpsD protein, E coli
  • kpsE protein, E coli
  • kpsM protein, E coli
  • kpsT protein, E coli
  • Polysaccharides, Bacterial