Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon

ABSTRACT The metabolism of lactate impacts infant gut health and may lead to acute accumulation of lactate and/or H2 associated with pain and crying of colicky infants. Because gut microbiota studies are limited due to ethical and safety concerns, in vitro fermentation models were developed as power...

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Autores principales:	Van Thanh Pham, Christophe Chassard, Etienne Rifa, Christian Braegger, Annelies Geirnaert, Vanesa Natalin Rocha Martin, Christophe Lacroix
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	in vitro model infant gut microbiota infantile colic lactate-utilizing bacteria pH retention time Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/134b21e2ce4843d2a7220e8ec8fa730b
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spelling	oai:doaj.org-article:134b21e2ce4843d2a7220e8ec8fa730b2021-12-02T18:25:16ZLactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon10.1128/mSystems.00264-182379-5077https://doaj.org/article/134b21e2ce4843d2a7220e8ec8fa730b2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00264-18https://doaj.org/toc/2379-5077ABSTRACT The metabolism of lactate impacts infant gut health and may lead to acute accumulation of lactate and/or H2 associated with pain and crying of colicky infants. Because gut microbiota studies are limited due to ethical and safety concerns, in vitro fermentation models were developed as powerful tools to assess effects of environmental conditions on the gut microbiota. In this study, we established a continuous colonic fermentation model (PolyFermS), inoculated with immobilized fecal microbiota and mimicking the proximal colon of 2-month-old infants. We investigated the effects of pH and retention time (RT) on lactate metabolism and of lactate-utilizing bacteria (LUB) exhibiting little or no H2 production. We observed that a drop in pH from 6.0 to 5.0 increased the number of lactate-producing bacteria (LPB) and decreased LUB concomitantly with lactate accumulation. Increasing RT from 5 to 10 h at pH 5.0 resulted in complete lactate consumption associated with increased LUB. Supplementation with dl-lactate (60 mM) to mimic lactate accumulation promoted propionate and butyrate production with no effect on acetate production. We further demonstrated that lactate-utilizing Propionibacterium avidum was able to colonize the reactors 4 days after spiking, suggesting its ability to compete with other lactate-utilizing bacteria producing H2. In conclusion, we showed that PolyFermS is a suitable model for mimicking young infant colonic microbiota. We report for the first time pH and RT as strong drivers for composition and metabolic activity of infant gut microbiota, especially for the metabolism of lactate, which is a key intermediate product for ecology and infant health. IMPORTANCE The metabolism of lactate is important for infant gut health and may lead to acute lactate and/or H2 accumulation, pain, and crying as observed in colicky infants. Functional human studies often faced ethical challenges due to invasive medical procedures; thus, in this study, we implemented PolyFermS fermentation models to mimic the infant proximal colon, which were inoculated with immobilized fecal microbiota of two 2-month-old infants. We investigated the impact of pH, retention time, and accumulation of dl-lactate on microbiota composition and metabolic activity. We found that a drop in pH from 6.0 to 5.0 led to increased LPB and decreased LUB concomitantly with lactate accumulation. Increasing the RT resulted in complete lactate consumption associated with increased LUB. Our data highlight for the first time the impact of key abiotic factors on the metabolism of lactate, which is an important intermediate product for ecology and infant health.Van Thanh PhamChristophe ChassardEtienne RifaChristian BraeggerAnnelies GeirnaertVanesa Natalin Rocha MartinChristophe LacroixAmerican Society for Microbiologyarticlein vitro modelinfant gut microbiotainfantile coliclactate-utilizing bacteriapHretention timeMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	in vitro model infant gut microbiota infantile colic lactate-utilizing bacteria pH retention time Microbiology QR1-502
spellingShingle	in vitro model infant gut microbiota infantile colic lactate-utilizing bacteria pH retention time Microbiology QR1-502 Van Thanh Pham Christophe Chassard Etienne Rifa Christian Braegger Annelies Geirnaert Vanesa Natalin Rocha Martin Christophe Lacroix Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
description	ABSTRACT The metabolism of lactate impacts infant gut health and may lead to acute accumulation of lactate and/or H2 associated with pain and crying of colicky infants. Because gut microbiota studies are limited due to ethical and safety concerns, in vitro fermentation models were developed as powerful tools to assess effects of environmental conditions on the gut microbiota. In this study, we established a continuous colonic fermentation model (PolyFermS), inoculated with immobilized fecal microbiota and mimicking the proximal colon of 2-month-old infants. We investigated the effects of pH and retention time (RT) on lactate metabolism and of lactate-utilizing bacteria (LUB) exhibiting little or no H2 production. We observed that a drop in pH from 6.0 to 5.0 increased the number of lactate-producing bacteria (LPB) and decreased LUB concomitantly with lactate accumulation. Increasing RT from 5 to 10 h at pH 5.0 resulted in complete lactate consumption associated with increased LUB. Supplementation with dl-lactate (60 mM) to mimic lactate accumulation promoted propionate and butyrate production with no effect on acetate production. We further demonstrated that lactate-utilizing Propionibacterium avidum was able to colonize the reactors 4 days after spiking, suggesting its ability to compete with other lactate-utilizing bacteria producing H2. In conclusion, we showed that PolyFermS is a suitable model for mimicking young infant colonic microbiota. We report for the first time pH and RT as strong drivers for composition and metabolic activity of infant gut microbiota, especially for the metabolism of lactate, which is a key intermediate product for ecology and infant health. IMPORTANCE The metabolism of lactate is important for infant gut health and may lead to acute lactate and/or H2 accumulation, pain, and crying as observed in colicky infants. Functional human studies often faced ethical challenges due to invasive medical procedures; thus, in this study, we implemented PolyFermS fermentation models to mimic the infant proximal colon, which were inoculated with immobilized fecal microbiota of two 2-month-old infants. We investigated the impact of pH, retention time, and accumulation of dl-lactate on microbiota composition and metabolic activity. We found that a drop in pH from 6.0 to 5.0 led to increased LPB and decreased LUB concomitantly with lactate accumulation. Increasing the RT resulted in complete lactate consumption associated with increased LUB. Our data highlight for the first time the impact of key abiotic factors on the metabolism of lactate, which is an important intermediate product for ecology and infant health.
format	article
author	Van Thanh Pham Christophe Chassard Etienne Rifa Christian Braegger Annelies Geirnaert Vanesa Natalin Rocha Martin Christophe Lacroix
author_facet	Van Thanh Pham Christophe Chassard Etienne Rifa Christian Braegger Annelies Geirnaert Vanesa Natalin Rocha Martin Christophe Lacroix
author_sort	Van Thanh Pham
title	Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
title_short	Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
title_full	Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
title_fullStr	Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
title_full_unstemmed	Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon
title_sort	lactate metabolism is strongly modulated by fecal inoculum, ph, and retention time in polyferms continuous colonic fermentation models mimicking young infant proximal colon
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/134b21e2ce4843d2a7220e8ec8fa730b
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Lactate Metabolism Is Strongly Modulated by Fecal Inoculum, pH, and Retention Time in PolyFermS Continuous Colonic Fermentation Models Mimicking Young Infant Proximal Colon

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