A unique in vivo experimental approach reveals metabolic adaptation of the probiotic Propionibacterium freudenreichii to the colon environment

Type Article
Date 2013-12
Language English
Author(s) Saraoui Taous1, 2, 6, Parayre Sandrine1, 2, Guernec Gregory3, 7, Loux Valentin4, Montfort Jerome3, Le Cam Aurelie3, Boudry Gaelle5, Jan G1, 2, Falentin Helene1, 2
Affiliation(s) 1 : INRA, UMR1253, F-35042 Rennes, France.
2 : AGROCAMPUS OUEST, UMR1253, F-35042 Rennes, France.
3 : INRA, UR1037, Lab Physiol & Genom Poissons, F-35000 Rennes, France.
4 : INRA, UR1077, F-78352 Jouy En Josas, France.
5 : INRA, UR1341, F-35590 St Gilles, France.
6 : IFREMER, Lab Sci & Technol Biomasse Marine, Nantes, France.
7 : Fac Med Toulouse, INSERM, UMR 1027, F-31073 Toulouse, France.
Source Bmc Genomics (1471-2164) (Biomed Central Ltd), 2013-12 , Vol. 14 , P. -
DOI 10.1186/1471-2164-14-911
WOS© Times Cited 23
Abstract Background

Propionibacterium freudenreichii is a food grade bacterium consumed both in cheeses and in probiotic preparations. Its promising probiotic potential, relying largely on the active release of beneficial metabolites within the gut as well as the expression of key surface proteins involved in immunomodulation, deserves to be explored more deeply. Adaptation to the colon environment is requisite for the active release of propionibacterial beneficial metabolites and constitutes a bottleneck for metabolic activity in vivo. Mechanisms allowing P. freudenreichii to adapt to digestive stresses have been only studied in vitro so far. Our aim was therefore to study P. freudenreichii metabolic adaptation to intra-colonic conditions in situ.

We maintained a pure culture of the type strain P. freudenreichii CIRM BIA 1, contained in a dialysis bag, within the colon of vigilant piglets during 24 hours. A transcriptomic analysis compared gene expression to identify the metabolic pathways induced by this environment, versus control cultures maintained in spent culture medium.

We observed drastic changes in the catabolism of sugars and amino-acids. Glycolysis, the Wood-Werkman cycle and the oxidative phosphorylation pathways were down-regulated but induction of specific carbohydrate catabolisms and alternative pathways were induced to produce NADH, NADPH, ATP and precursors (utilizing of propanediol, gluconate, lactate, purine and pyrimidine and amino-acids). Genes involved in stress response were down-regulated and genes specifically expressed during cell division were induced, suggesting that P. freudenreichii adapted its metabolism to the conditions encountered in the colon.

This study constitutes the first molecular demonstration of P. freudenreichii activity and physiological adaptation in vivo within the colon. Our data are likely specific to our pig microbiota composition but opens an avenue towards understanding probiotic action within the gut in further studies comparing bacterial adaptation to different microbiota.
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Saraoui Taous, Parayre Sandrine, Guernec Gregory, Loux Valentin, Montfort Jerome, Le Cam Aurelie, Boudry Gaelle, Jan G, Falentin Helene (2013). A unique in vivo experimental approach reveals metabolic adaptation of the probiotic Propionibacterium freudenreichii to the colon environment. Bmc Genomics, 14, -. Publisher's official version : https://doi.org/10.1186/1471-2164-14-911 , Open Access version : https://archimer.ifremer.fr/doc/00171/28205/