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Impact of the Metabolic Activity of Streptococcus thermophilus on the Colon Epithelium of Gnotobiotic Rats*

  • 2011-03
  • Journal of Biological Chemistry 286(12)
    • F. Rul
    • L. Ben-Yahia
    • F. Chegdani
    • Laura Wrzosek
    • Stéphane Thomas
    • Marie‐Louise Noordine
    • C. Gitton
    • C. Cherbuy
    • P. Langella
    • Muriel Thomas

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.

Research Insights

SupplementHealth OutcomeEffect TypeEffect Size
Streptococcus thermophilusIncreased Abundance of Cell Cycle Arrest Protein p27(Kip1)Neutral
Moderate
Streptococcus thermophilusInduced Glycolysis Pathway in Gastrointestinal TractNeutral
Moderate
Streptococcus thermophilus MAK34S24TIncreased Cell Cycle Arrest Protein LevelsNeutral
Moderate
Streptococcus thermophilus NBRC 13957Increased Abundance of Cell Cycle Arrest Protein p27(Kip1)Neutral
Moderate
Streptococcus thermophilus NBRC 13957Increased Glycolysis Pathway ActivityNeutral
Large
Streptococcus thermophilus NBRC 13957Increased Monocarboxylic Acid Transporter mRNAsNeutral
Moderate
Streptococcus thermophilus PXN 66Increased Lactate LevelsNeutral
Moderate
Streptococcus thermophilus PXN 66Increased p27(Kip1) Protein LevelsNeutral
Moderate
Streptococcus thermophilus SEBioticIncreased Cecal Glycolysis Leading to Elevated LactateNeutral
Moderate
Streptococcus thermophilus SEBioticModulation of Colon Epithelium by LactateNeutral
Moderate
Streptococcus thermophilus SL-21Altered Gene Expression in Colon EpitheliumNeutral
Moderate
Streptococcus thermophilus SL-21Increased Lactate LevelsNeutral
Moderate
Streptococcus thermophilus SP4Increased Monocarboxylic Acid Transporter mRNAsNeutral
Moderate
Streptococcus thermophilus SP4Increased p27(Kip1) Protein LevelsNeutral
Moderate
Streptococcus thermophilus ST-21Increased Cell Cycle Arrest Protein LevelsNeutral
Moderate
Streptococcus thermophilus ST-21Increased Monocarboxylic Acid Transporter mRNA LevelsNeutral
Moderate
Streptococcus thermophilus VPro 23Enhanced Glycolysis Pathway ActivationNeutral
Moderate
Streptococcus thermophilus VPro 23Increased Monocarboxylic Acid Transporter mRNAsNeutral
Moderate
Streptococcus thermophilus VPro 23Induced Cell Cycle ArrestNeutral
Moderate
Streptococcus thermophilus Y08 AFEnhanced Glycolysis Pathway ActivationNeutral
Moderate
Streptococcus thermophilus Y08 AFIncreased Cell Cycle Arrest Protein LevelsNeutral
Moderate
Streptococcus thermophilus Y08 AFIncreased Monocarboxylic Acid Transporter mRNAsNeutral
Moderate

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