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Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome

Propionibacterium freudenreichii is a beneficial bacterium that modulates the gut microbiota, motility and inflammation. It is traditionally consumed within various fermented dairy products. Changes to consumer habits in the context of food transition are, however, driving the demand for non-dairy f...

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Autores principales: Tarnaud, Florian, Gaucher, Floriane, do Carmo, Fillipe Luiz Rosa, Illikoud, Nassima, Jardin, Julien, Briard-Bion, Valérie, Guyomarc’h, Fanny, Gagnaire, Valérie, Jan, Gwénaël
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7736159/
https://www.ncbi.nlm.nih.gov/pubmed/33335514
http://dx.doi.org/10.3389/fmicb.2020.549027
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author Tarnaud, Florian
Gaucher, Floriane
do Carmo, Fillipe Luiz Rosa
Illikoud, Nassima
Jardin, Julien
Briard-Bion, Valérie
Guyomarc’h, Fanny
Gagnaire, Valérie
Jan, Gwénaël
author_facet Tarnaud, Florian
Gaucher, Floriane
do Carmo, Fillipe Luiz Rosa
Illikoud, Nassima
Jardin, Julien
Briard-Bion, Valérie
Guyomarc’h, Fanny
Gagnaire, Valérie
Jan, Gwénaël
author_sort Tarnaud, Florian
collection PubMed
description Propionibacterium freudenreichii is a beneficial bacterium that modulates the gut microbiota, motility and inflammation. It is traditionally consumed within various fermented dairy products. Changes to consumer habits in the context of food transition are, however, driving the demand for non-dairy fermented foods, resulting in a considerable development of plant-based fermented products that require greater scientific knowledge. Fermented soymilks, in particular, offer an alternative source of live probiotics. While the adaptation of lactic acid bacteria (LAB) to such vegetable substrates is well documented, little is known about that of propionibacteria. We therefore investigated the adaptation of Propionibacterium freudenreichii to soymilk by comparison to cow’s milk. P. freudenreichii grew in cow’s milk but not in soymilk, but it did grow in soymilk when co-cultured with the lactic acid bacterium Lactobacillus plantarum. When grown in soymilk ultrafiltrate (SUF, the aqueous phase of soymilk), P. freudenreichii cells appeared thinner and rectangular-shaped, while they were thicker and more rounded in cow’s milk utltrafiltrate (MUF, the aqueous phase of cow milk). The amount of extractable surface proteins (SlpA, SlpB, SlpD, SlpE) was furthermore reduced in SUF, when compared to MUF. This included the SlpB protein, previously shown to modulate adhesion and immunomodulation in P. freudenreichii. Tolerance toward an acid and toward a bile salts challenge were enhanced in SUF. By contrast, tolerance toward an oxidative and a thermal challenge were enhanced in MUF. A whole-cell proteomic approach further identified differential expression of 35 proteins involved in amino acid transport and metabolism (including amino acid dehydrogenase, amino acid transporter), 32 proteins involved in carbohydrate transport and metabolism (including glycosyltransferase, PTS), indicating metabolic adaptation to the substrate. The culture medium also modulated the amount of stress proteins involved in stress remediation: GroEL, OpuCA, CysK, DnaJ, GrpE, in line with the modulation of stress tolerance. Changing the fermented substrate may thus significantly affect the fermentative and probiotic properties of dairy propionibacteria. This needs to be considered when developing new fermented functional foods.
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spelling pubmed-77361592020-12-16 Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome Tarnaud, Florian Gaucher, Floriane do Carmo, Fillipe Luiz Rosa Illikoud, Nassima Jardin, Julien Briard-Bion, Valérie Guyomarc’h, Fanny Gagnaire, Valérie Jan, Gwénaël Front Microbiol Microbiology Propionibacterium freudenreichii is a beneficial bacterium that modulates the gut microbiota, motility and inflammation. It is traditionally consumed within various fermented dairy products. Changes to consumer habits in the context of food transition are, however, driving the demand for non-dairy fermented foods, resulting in a considerable development of plant-based fermented products that require greater scientific knowledge. Fermented soymilks, in particular, offer an alternative source of live probiotics. While the adaptation of lactic acid bacteria (LAB) to such vegetable substrates is well documented, little is known about that of propionibacteria. We therefore investigated the adaptation of Propionibacterium freudenreichii to soymilk by comparison to cow’s milk. P. freudenreichii grew in cow’s milk but not in soymilk, but it did grow in soymilk when co-cultured with the lactic acid bacterium Lactobacillus plantarum. When grown in soymilk ultrafiltrate (SUF, the aqueous phase of soymilk), P. freudenreichii cells appeared thinner and rectangular-shaped, while they were thicker and more rounded in cow’s milk utltrafiltrate (MUF, the aqueous phase of cow milk). The amount of extractable surface proteins (SlpA, SlpB, SlpD, SlpE) was furthermore reduced in SUF, when compared to MUF. This included the SlpB protein, previously shown to modulate adhesion and immunomodulation in P. freudenreichii. Tolerance toward an acid and toward a bile salts challenge were enhanced in SUF. By contrast, tolerance toward an oxidative and a thermal challenge were enhanced in MUF. A whole-cell proteomic approach further identified differential expression of 35 proteins involved in amino acid transport and metabolism (including amino acid dehydrogenase, amino acid transporter), 32 proteins involved in carbohydrate transport and metabolism (including glycosyltransferase, PTS), indicating metabolic adaptation to the substrate. The culture medium also modulated the amount of stress proteins involved in stress remediation: GroEL, OpuCA, CysK, DnaJ, GrpE, in line with the modulation of stress tolerance. Changing the fermented substrate may thus significantly affect the fermentative and probiotic properties of dairy propionibacteria. This needs to be considered when developing new fermented functional foods. Frontiers Media S.A. 2020-12-01 /pmc/articles/PMC7736159/ /pubmed/33335514 http://dx.doi.org/10.3389/fmicb.2020.549027 Text en Copyright © 2020 Tarnaud, Gaucher, do Carmo, Illikoud, Jardin, Briard-Bion, Guyomarc’h, Gagnaire and Jan. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Tarnaud, Florian
Gaucher, Floriane
do Carmo, Fillipe Luiz Rosa
Illikoud, Nassima
Jardin, Julien
Briard-Bion, Valérie
Guyomarc’h, Fanny
Gagnaire, Valérie
Jan, Gwénaël
Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title_full Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title_fullStr Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title_full_unstemmed Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title_short Differential Adaptation of Propionibacterium freudenreichii CIRM-BIA129 to Cow’s Milk Versus Soymilk Environments Modulates Its Stress Tolerance and Proteome
title_sort differential adaptation of propionibacterium freudenreichii cirm-bia129 to cow’s milk versus soymilk environments modulates its stress tolerance and proteome
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7736159/
https://www.ncbi.nlm.nih.gov/pubmed/33335514
http://dx.doi.org/10.3389/fmicb.2020.549027
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