Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>

ABSTRACT The gut microbiota contributes to nutrients absorption and metabolism by enterocytes, but the molecular mechanisms involved remain poorly understood, and most conclusions are inferred from studies comparing germfree and conventional animals colonized with diverse bacterial species. We selec...

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Autores principales:	Asmaa Tazi, João Ricardo Araujo, Céline Mulet, Ellen T. Arena, Giulia Nigro, Thierry Pédron, Philippe J. Sansonetti
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Escherichia coli Lactobacillus chylomicrons high-fat diet lipid metabolism microbiota Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b022de92f42f4ebd9d79c8e7ee9bd710
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spelling	oai:doaj.org-article:b022de92f42f4ebd9d79c8e7ee9bd7102021-11-15T15:58:21ZDisentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>10.1128/mBio.01493-182150-7511https://doaj.org/article/b022de92f42f4ebd9d79c8e7ee9bd7102018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01493-18https://doaj.org/toc/2150-7511ABSTRACT The gut microbiota contributes to nutrients absorption and metabolism by enterocytes, but the molecular mechanisms involved remain poorly understood, and most conclusions are inferred from studies comparing germfree and conventional animals colonized with diverse bacterial species. We selected two model commensal microorganisms, Escherichia coli and Lactobacillus paracasei, to assess the role of the small-intestinal microbiota in modulating lipid absorption and metabolism by the epithelium. Using an integrated approach encompassing cellular and murine models and combining metabolic parameters measurement, lipid droplet imaging, and gene expression analysis, we demonstrated that under homeostatic conditions, L. paracasei promotes fat storage in enterocytes, whereas E. coli enhances lipid catabolism and reduces chylomicron circulating levels. The Akt/mammalian target of sirolimus (mTOR) pathway is inhibited by both bacterial species in vitro, indicating that several regulatory pathways are involved in the distinct intracellular lipid outcomes associated with each bacterial species. Moreover, soluble bacterial factors partially reproduce the effects observed with live microorganisms. However, reduction of chylomicron circulating levels in E. coli-colonized animals is lost under high-fat-diet conditions, whereas it is potentiated by L. paracasei colonization accompanied by resistance to hypercholesterolemia and excess body weight gain. IMPORTANCE The specific contribution of each bacterial species within a complex microbiota to the regulation of host lipid metabolism remains largely unknown. Using two model commensal microorganisms, L. paracasei and E. coli, we demonstrated that both bacterial species impacted host lipid metabolism in a diet-dependent manner and, notably, that L. paracasei-colonized mice but not E. coli-colonized mice resisted high-fat-diet-induced body weight gain. In addition, we set up cellular models of fatty acid absorption and secretion by enterocytes cocultured with bacteria and showed that, in vitro, both L. paracasei and E. coli inhibited lipid secretion, through increased intracellular fat storage and enhanced lipid catabolism, respectively.Asmaa TaziJoão Ricardo AraujoCéline MuletEllen T. ArenaGiulia NigroThierry PédronPhilippe J. SansonettiAmerican Society for MicrobiologyarticleEscherichia coliLactobacilluschylomicronshigh-fat dietlipid metabolismmicrobiotaMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli Lactobacillus chylomicrons high-fat diet lipid metabolism microbiota Microbiology QR1-502
spellingShingle	Escherichia coli Lactobacillus chylomicrons high-fat diet lipid metabolism microbiota Microbiology QR1-502 Asmaa Tazi João Ricardo Araujo Céline Mulet Ellen T. Arena Giulia Nigro Thierry Pédron Philippe J. Sansonetti Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
description	ABSTRACT The gut microbiota contributes to nutrients absorption and metabolism by enterocytes, but the molecular mechanisms involved remain poorly understood, and most conclusions are inferred from studies comparing germfree and conventional animals colonized with diverse bacterial species. We selected two model commensal microorganisms, Escherichia coli and Lactobacillus paracasei, to assess the role of the small-intestinal microbiota in modulating lipid absorption and metabolism by the epithelium. Using an integrated approach encompassing cellular and murine models and combining metabolic parameters measurement, lipid droplet imaging, and gene expression analysis, we demonstrated that under homeostatic conditions, L. paracasei promotes fat storage in enterocytes, whereas E. coli enhances lipid catabolism and reduces chylomicron circulating levels. The Akt/mammalian target of sirolimus (mTOR) pathway is inhibited by both bacterial species in vitro, indicating that several regulatory pathways are involved in the distinct intracellular lipid outcomes associated with each bacterial species. Moreover, soluble bacterial factors partially reproduce the effects observed with live microorganisms. However, reduction of chylomicron circulating levels in E. coli-colonized animals is lost under high-fat-diet conditions, whereas it is potentiated by L. paracasei colonization accompanied by resistance to hypercholesterolemia and excess body weight gain. IMPORTANCE The specific contribution of each bacterial species within a complex microbiota to the regulation of host lipid metabolism remains largely unknown. Using two model commensal microorganisms, L. paracasei and E. coli, we demonstrated that both bacterial species impacted host lipid metabolism in a diet-dependent manner and, notably, that L. paracasei-colonized mice but not E. coli-colonized mice resisted high-fat-diet-induced body weight gain. In addition, we set up cellular models of fatty acid absorption and secretion by enterocytes cocultured with bacteria and showed that, in vitro, both L. paracasei and E. coli inhibited lipid secretion, through increased intracellular fat storage and enhanced lipid catabolism, respectively.
format	article
author	Asmaa Tazi João Ricardo Araujo Céline Mulet Ellen T. Arena Giulia Nigro Thierry Pédron Philippe J. Sansonetti
author_facet	Asmaa Tazi João Ricardo Araujo Céline Mulet Ellen T. Arena Giulia Nigro Thierry Pédron Philippe J. Sansonetti
author_sort	Asmaa Tazi
title	Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
title_short	Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
title_full	Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
title_fullStr	Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
title_full_unstemmed	Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>
title_sort	disentangling host-microbiota regulation of lipid secretion by enterocytes: insights from commensals <italic toggle="yes">lactobacillus paracasei</italic> and <italic toggle="yes">escherichia coli</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/b022de92f42f4ebd9d79c8e7ee9bd710
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Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals <italic toggle="yes">Lactobacillus paracasei</italic> and <italic toggle="yes">Escherichia coli</italic>

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