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. Streptococcus thermophilus 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 S. thermophilus on the mucus by evaluating its ability to adhere, degrade, modify, or induce the production of mucus and/or mucins. Adhesion was analyzed in vitro 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 S. thermophilus is the unique bacterial species in the digestive tract or transited as a sub-dominant bacterium through a complex microbiota. S. thermophilus 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 Lactococcus lactis. The presence of S. thermophilus 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 S. thermophilus via 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 S. thermophilus is a poor mucus-adhesive bacterium, it can promote mucus pathway at least in part by producing lactate in the digestive tract.

Antilisterial Potential of Lactic Acid Bacteria in Eliminating Listeria monocytogenes in Host and Ready-to-Eat Food Application

“…For instance, Lactobacillus casei and L reuteri only significantly elevated MUC2 and TFF3 genes' expression, respectively; L. rhamnosus significantly augmented MUC2 and GAL3ST2; L. fermentum expressed the TFF3 gene to peak at 24 h. Besides, certain cell-free supernatants (CFS) of LAB were also shown to upregulate these genes' expression, illustrating that specific compounds produced by LAB may be involved in goblet cell function modulation, which is supported by Caballero-Franco et al (2007) [91]. It is also in line with Fernandez et al [92], who reported that lactate produced from S. thermophilus was suggested to upregulate KLF4 protein involved in goblet cell differentiation maturation, despite weak adhesion of S. thermophilus onto the mucus layer of HT-29 cells. Interaction of lactate and Gpr81 (G-protein-coupled receptor) in the intestine stimulates intestinal stem cells, thereby maintaining IECs' integrity [93].…”

Experimental models to study intestinal microbes–mucus interactions in health and disease

“…Representative members of the two main phyla of the gut microbiota, B. thetaiotaomicron and Faecalibacterium prauznitzii can modulate goblet cell differentiation and thus mucus production (Wrzosek et al, 2013). A recent study showed that Streptococcus thermophilus, a transient food-borne bacterium, was able to induce mucus pathway in gnotobiotic rodents despite its poor capacity for mucus adhesion and mucin glycan degradation in vitro (Fernandez et al, 2018). Some of the mechanisms mediating mucin production and secretion by gut bacteria have been elucidated as described below.…”

“…The effect of butyrate on MUC2 gene expression is mediated by epigenetic modifications (acetylation/methylation of histones) on the MUC2 promoter as demonstrated in vitro using human goblet cell-like LS174T cells (Burger-van Paassen et al, 2009). Fernandez and colleagues suggested that lactate produced by S. thermophilus in the GI tract could stimulate mucus production via a signalling pathway dependent of KLF4, a transcription factor involved in the differentiation of goblet cells (Fernandez et al, 2018). Some other bacterial effectors have been identified to mediate mucin expression and glycosylation such as small peptides from R. gnavus and B.…”

Short-chain fatty acid administration via water acidifier improves feed efficiency and modulates fecal microbiota in weaned piglets

“…Streptococcus belong to the lactic acid bacteria. Some species have probiotic characteristics ( Zhou et al, 2016 ; Fernandez et al, 2018 ); however, they are generally associated with pathogenic bacteria ( Köhler, 2007 ; Moreno et al, 2016 ). The most important pathogenic species for the pig industry is Streptococcus suis , which is the cause of various diseases such as meningitis, septicemia, and endocarditis ( Moreno et al, 2016 ; Murase et al, 2019 ).…”