Characterization of Mucus-Related Properties of Streptococcus thermophilus: From Adhesion to Induction

Abstract

Mucus is a major component of the intestinal barrier involved both in the protection of the host and the fitness of commensals of the gut. <i>Streptococcus thermophilus</i> is consumed world-wide in fermented dairy products and is also recognized as a probiotic, as its consumption is associated with improved lactose digestion. We determined the overall effect of <i>S. thermophilus</i> on the mucus by evaluating its ability to adhere, degrade, modify, or induce the production of mucus and/or mucins. Adhesion was analyzed <i>in vitro</i> using two types of mucins (from pig or human biopsies) and mucus-producing intestinal HT29-MTX cells. The induction of mucus was characterized in two different rodent models, in which <i>S. thermophilus</i> is the unique bacterial species in the digestive tract or transited as a sub-dominant bacterium through a complex microbiota. <i>S. thermophilus</i> LMD-9 and LMG18311 strains did not grow in sugars used to form mucins as the sole carbon source and displayed weak binding to mucus/mucins relative to the highly adhesive TIL448 <i>Lactococcus lactis</i>. The presence of <i>S. thermophilus</i> as the unique bacteria in the digestive tract of gnotobiotic rats led to accumulation of lactate and increased the number of Alcian-Blue positive goblet cells and the amount of the mucus-inducer KLF4 transcription factor. Lactate significantly increased KLF4 protein levels in HT29-MTX cells. Introduction of <i>S. thermophilus</i><i>via</i> transit as a sub-dominant bacterium (10³ CFU/g feces) in a complex endogenous microbiota resulted in a slight increase in lactate levels in the digestive tract, no induction of overall mucus production, and moderate induction of sulfated mucin production. We thus show that although <i>S. thermophilus</i> is a poor mucus-adhesive bacterium, it can promote mucus pathway at least in part by producing lactate in the digestive tract.