Abstract
The thermophilic lactic acid bacterium Streptococcus thermophilus is widely and traditionally used in the dairy industry. Despite the vast level of consumption of S. thermophilus through yogurt or probiotic functional food, very few data are available about its physiology in the gastrointestinal tract (GIT). The objective of the present work was to explore both the metabolic activity and host response of S. thermophilus in vivo. Our study profiles the protein expression of S. thermophilus after its adaptation to the GIT of gnotobiotic rats and describes the impact of S. thermophilus colonization on the colonic epithelium. S. thermophilus colonized progressively the GIT of germ-free rats to reach a stable population in 30 days (10(8) cfu/g of feces). This progressive colonization suggested that S. thermophilus undergoes an adaptation process within GIT. Indeed, we showed that the main response of S. thermophilus in the rat's GIT was the massive induction of the glycolysis pathway, leading to formation of lactate in the cecum. At the level of the colonic epithelium, the abundance of monocarboxylic acid transporter mRNAs (SLC16A1 and SLC5A8) and a protein involved in the cell cycle arrest (p27(kip1)) increased in the presence of S. thermophilus compared with germ-free rats. Based on different mono-associated rats harboring two different strains of S. thermophilus (LMD-9 or LMG18311) or weak lactate-producing commensal bacteria (Bacteroides thetaiotaomicron and Ruminococcus gnavus), we propose that lactate could be a signal produced by S. thermophilus and modulating the colon epithelium.
Highlights
Trointestinal tract (GIT)3 through their lactose-hydrolyzing activity present in yogurt and in the gastrointestinal tract (GIT), reducing symptoms of lactose intolerance [2, 3]
The implantation of S. thermophilus LMD-9 occurred in a three-step way: 1) initiation phase with implantation of 105 cfu/g of feces; 2) growth period between weeks 2 and 3, where it reached a population of 108 cfu/g of feces; and 3) maintenance phase
To mimic the levels present in yogurt, GF rats were inoculated with a co-culture containing 109 cfu/ml S. thermophilus LMD-9 and 107 cfu/ml L. bulgaricus, in accordance with the relative proportion of both strains in yogurt. 24 h after gavage, L. bulgaricus was undetectable in feces, whereas the implantation curve of S. thermophilus LMD-9 was similar to that observed with Ino-LMD9
Summary
Trointestinal tract (GIT) through their lactose-hydrolyzing activity present in yogurt and in the GIT, reducing symptoms of lactose intolerance [2, 3]. Recent data indicate that strains related to S. thermophilus LMD-9 are among the 57 bacteria species found in the intestinal microbiota of 90% of 124 European individuals [7]. The Streptococcus genus, with in some studies a precision at the level of S. thermophilus species, is among the first colonizers of the GIT because it has been detected in infant feces and breast milk [11,12,13]. We have recently demonstrated that microbiota increases colonic epithelium crypt depth in concordance with a well orchestrated modulation of the level of proteins involved in life cycle steps like PCNA, Bcl, and p21cip, p27kip (markers of proliferation, antiapoptotic pathway, and cell cycle arrest, respectively) [17]. In view of our findings using different mono-associated models, we propose that lactate resulting from the adaptive metabolic activity of S. thermophilus may serve as a biological signal to communicate with host epithelium
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