Crystal structure of lactobacillar SpaC reveals an atypical five-domain pilus tip adhesin: Exposing its substrate-binding and assembly in SpaCBA pili

J Struct Biol. 2020 Sep 1;211(3):107571. doi: 10.1016/j.jsb.2020.107571. Epub 2020 Jul 10.

Abstract

Adhesion to cell surfaces is an essential and early prerequisite for successful host colonization by bacteria, and in most instances involves the specificities of various adhesins. Among bacterial Gram-positives, some genera and species mediate attachment to host cells by using long non-flagellar appendages called sortase-dependent pili. A case in point is the beneficial Lactobacillus rhamnosus GG gut-adapted strain that produces the so-called SpaCBA pilus, a structure noted for its promiscuous binding to intestinal mucus and collagen. Structurally, SpaCBA pili are heteropolymers of three different pilin-protein subunits, each with its own location and function in the pilus: backbone SpaA for length, basal SpaB for anchoring, and tip SpaC for adhesion. Previously, we solved the SpaA tertiary structure by X-ray crystallography and also reported on the crystallization of SpaB and SpaC. Here, we reveal the full-length high-resolution (1.9 Å) crystal structure of SpaC, a first for a sortase-dependent pilus-bearing commensal. The SpaC structure, unlike the representative four-domain architecture of other Gram-positive tip pilins, espouses an atypically longer five-domain arrangement that includes N-terminal 'binding' and C-terminal 'stalk' regions of two and three domains, respectively. With the prospect of establishing new mechanistic insights, we provide a structural basis for the multi-substrate binding nature of SpaC, as well as a structural model that reconciles its exclusive localization at the SpaCBA pilus tip.

Keywords: Adhesion; Collagen; Lactobacillus rhamnosus GG; Lectin; Mucin; Probiotics; Sortase-dependent pili; Tip pilin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Binding Sites
  • Collagen / metabolism
  • Crystallography, X-Ray
  • Fimbriae, Bacterial / chemistry*
  • Fimbriae, Bacterial / metabolism
  • Lacticaseibacillus rhamnosus / chemistry*
  • Lacticaseibacillus rhamnosus / cytology
  • Membrane Proteins / chemistry*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Microscopy, Atomic Force
  • Microscopy, Immunoelectron
  • Models, Molecular
  • Molecular Docking Simulation
  • Protein Domains

Substances

  • Bacterial Proteins
  • Membrane Proteins
  • SpaC protein, bacteria
  • Collagen