Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>

ABSTRACT The aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut. Hence, different Fe availabilities were mimicked in an in vitro colonic fermentation model (the polyfermenter intestinal model called Pol...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Alexandra Dostal, Christophe Lacroix, Lea Bircher, Van Thanh Pham, Rainer Follador, Michael Bruce Zimmermann, Christophe Chassard
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d30c5d8624e642d8a9b284c5c0730222
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d30c5d8624e642d8a9b284c5c0730222
record_format	dspace
spelling	oai:doaj.org-article:d30c5d8624e642d8a9b284c5c07302222021-11-15T15:41:23ZIron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>10.1128/mBio.01453-152150-7511https://doaj.org/article/d30c5d8624e642d8a9b284c5c07302222015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01453-15https://doaj.org/toc/2150-7511ABSTRACT The aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut. Hence, different Fe availabilities were mimicked in an in vitro colonic fermentation model (the polyfermenter intestinal model called PolyFermS) inoculated with immobilized gut microbiota from a child and in batch cultures of the butyrate producer Roseburia intestinalis. Shifts in the microbial community (16S rRNA sequencing and quantitative PCR), metabolic activity (high-performance liquid chromatography), and expression of genes involved in butyrate production were assessed. In the PolyFermS, moderate Fe deficiency resulted in a 1.4-fold increase in butyrate production and a 5-fold increase in butyryl-coenzyme A (CoA):acetate CoA-transferase gene expression, while very strong Fe deficiency significantly decreased butyrate concentrations and butyrate-producing bacteria compared with the results under normal Fe conditions. Batch cultures of R. intestinalis grown in a low-Fe environment preferentially produced lactate and had reduced butyrate and hydrogen production, in parallel with upregulation of the lactate dehydrogenase gene and downregulation of the pyruvate:ferredoxin-oxidoreductase gene. In contrast, under high-Fe conditions, R. intestinalis cultures showed enhanced butyrate and hydrogen production, along with increased expression of the corresponding genes, compared with the results under normal-Fe conditions. Our data reveal the strong regulatory effect of Fe on gut microbiota butyrate producers and on the concentrations of butyrate, which contributes to the maintenance of host gut health. IMPORTANCE Fe deficiency is one of the most common nutritional deficiencies worldwide and can be corrected by Fe supplementation. In this in vitro study, we show that environmental Fe concentrations in a continuous gut fermentation model closely mimicking a child's gut microbiota strongly affect the composition of the gut microbiome and its metabolic activity, particularly butyrate production. The differential expression of genes involved in the butyrate production pathway under different Fe conditions and the enzyme cofactor role of Fe explain the observed modulation of butyrate production. Our data reveal that the level of dietary Fe reaching the colon affects the microbiome, and its essential function of providing the host with beneficial butyrate.Alexandra DostalChristophe LacroixLea BircherVan Thanh PhamRainer FolladorMichael Bruce ZimmermannChristophe ChassardAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Alexandra Dostal Christophe Lacroix Lea Bircher Van Thanh Pham Rainer Follador Michael Bruce Zimmermann Christophe Chassard Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
description	ABSTRACT The aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut. Hence, different Fe availabilities were mimicked in an in vitro colonic fermentation model (the polyfermenter intestinal model called PolyFermS) inoculated with immobilized gut microbiota from a child and in batch cultures of the butyrate producer Roseburia intestinalis. Shifts in the microbial community (16S rRNA sequencing and quantitative PCR), metabolic activity (high-performance liquid chromatography), and expression of genes involved in butyrate production were assessed. In the PolyFermS, moderate Fe deficiency resulted in a 1.4-fold increase in butyrate production and a 5-fold increase in butyryl-coenzyme A (CoA):acetate CoA-transferase gene expression, while very strong Fe deficiency significantly decreased butyrate concentrations and butyrate-producing bacteria compared with the results under normal Fe conditions. Batch cultures of R. intestinalis grown in a low-Fe environment preferentially produced lactate and had reduced butyrate and hydrogen production, in parallel with upregulation of the lactate dehydrogenase gene and downregulation of the pyruvate:ferredoxin-oxidoreductase gene. In contrast, under high-Fe conditions, R. intestinalis cultures showed enhanced butyrate and hydrogen production, along with increased expression of the corresponding genes, compared with the results under normal-Fe conditions. Our data reveal the strong regulatory effect of Fe on gut microbiota butyrate producers and on the concentrations of butyrate, which contributes to the maintenance of host gut health. IMPORTANCE Fe deficiency is one of the most common nutritional deficiencies worldwide and can be corrected by Fe supplementation. In this in vitro study, we show that environmental Fe concentrations in a continuous gut fermentation model closely mimicking a child's gut microbiota strongly affect the composition of the gut microbiome and its metabolic activity, particularly butyrate production. The differential expression of genes involved in the butyrate production pathway under different Fe conditions and the enzyme cofactor role of Fe explain the observed modulation of butyrate production. Our data reveal that the level of dietary Fe reaching the colon affects the microbiome, and its essential function of providing the host with beneficial butyrate.
format	article
author	Alexandra Dostal Christophe Lacroix Lea Bircher Van Thanh Pham Rainer Follador Michael Bruce Zimmermann Christophe Chassard
author_facet	Alexandra Dostal Christophe Lacroix Lea Bircher Van Thanh Pham Rainer Follador Michael Bruce Zimmermann Christophe Chassard
author_sort	Alexandra Dostal
title	Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_short	Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_full	Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_fullStr	Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_full_unstemmed	Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_sort	iron modulates butyrate production by a child gut microbiota <italic toggle="yes">in vitro</italic>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/d30c5d8624e642d8a9b284c5c0730222
work_keys_str_mv	AT alexandradostal ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT christophelacroix ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT leabircher ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT vanthanhpham ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT rainerfollador ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT michaelbrucezimmermann ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic AT christophechassard ironmodulatesbutyrateproductionbyachildgutmicrobiotaitalictoggleyesinvitroitalic
_version_	1718427731870351360

Iron Modulates Butyrate Production by a Child Gut Microbiota <italic toggle="yes">In Vitro</italic>

Ejemplares similares