Streptococcus gordonii Poised for Glycan Feeding
through a MUC5…ediated Outside-In Signaling Circuit
ASM Journals / Journal of Bacteriology / Ahead of
Print https://journals.asm.org/doi/10.1128/jb.00118-22
ABSTRACT :Many oral bacteria
employ cell wall-anchored adhesins to bind to the salivary films coating the teeth
and mucosal surfaces. Surface binding prevents clearance and facilitates
catabolism of salivary film glycoproteins. We asked whether Streptococcus
gordonii adhesion expression changes in response to surface salivary cues using
a eukaryote-like, outside-in recognition and signaling circuit. To determine
whether the cues were discriminated, S. gordonii was tested during cell
adhesion and biofilm formation on a MUC5B-rich or lower-molecular-mass salivary
fraction or an uncoated abiotic surface. Cells were recovered and analyzed for
differences in gene expression and proteins in cell wall fractions. In salivary-free
conditions, planktonic S. gordonii presented three prominent cell wall
LPXTG-motif proteins, SGO_1487, SGO_0890, and MbpA (mucin-binding protein A;
SGO_0707). During biofilm formation on MUC5B-coated surfaces, MbpA, a
MUC5B-binding protein, and key genes in the tagatose and quorum-sensing
pathways were strongly promoted. The response to MUC5B required the
two-component system (TCS),streptococcal regulator of adhesins sensor and
regulator (SraSR,SGO_1180/81), lipoteichoic acid (LTA), and the homologous
paired adhesins, SspA and SspB (SspAB). LTA appears to link the outside signal(MUC5B)
to intramembrane SraSR. Tagatose pathway gene expression may poise cells to
metabolize MUC5B glycans and, with a quorum-sensing gene (luxS), may direct
formation of a consortium to facilitate glycan cross-feeding by S. gordonii. We
now show that a Gram-positive bacterium discriminates specific surface
environmental cues using an outside-in signaling mechanism to apparently
optimize colonization of saliva-coated surfaces.