<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals

ABSTRACT Therapeutically active glycosylated phytochemicals are ubiquitous in the human diet. The human gut microbiota (HGM) modulates the bioactivities of these compounds, which consequently affect host physiology and microbiota composition. Despite a significant impact on human health, the key pla...

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Autores principales:	Mia C. Theilmann, Yong Jun Goh, Kristian Fog Nielsen, Todd R. Klaenhammer, Rodolphe Barrangou, Maher Abou Hachem
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Lactobacillus beta-glucoside bioavailability gut microbiota phytochemical polydatin Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c272d79e522f4bdca314091d9e187d49
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spelling	oai:doaj.org-article:c272d79e522f4bdca314091d9e187d492021-11-15T15:51:56Z<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals10.1128/mBio.01421-172150-7511https://doaj.org/article/c272d79e522f4bdca314091d9e187d492017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01421-17https://doaj.org/toc/2150-7511ABSTRACT Therapeutically active glycosylated phytochemicals are ubiquitous in the human diet. The human gut microbiota (HGM) modulates the bioactivities of these compounds, which consequently affect host physiology and microbiota composition. Despite a significant impact on human health, the key players and the underpinning mechanisms of this interplay remain uncharacterized. Here, we demonstrate the growth of Lactobacillus acidophilus on mono- and diglucosyl dietary plant glycosides (PGs) possessing small aromatic aglycones. Transcriptional analysis revealed the upregulation of host interaction genes and identified two loci that encode phosphotransferase system (PTS) transporters and phospho-β-glucosidases, which mediate the uptake and deglucosylation of these compounds, respectively. Inactivating these transport and hydrolysis genes abolished or severely reduced growth on PG, establishing the specificity of the loci to distinct groups of PGs. Following intracellular deglucosylation, the aglycones of PGs are externalized, rendering them available for absorption by the host or for further modification by other microbiota taxa. The PG utilization loci are conserved in L. acidophilus and closely related lactobacilli, in correlation with versatile growth on these compounds. Growth on the tested PG appeared more common among human gut lactobacilli than among counterparts from other ecologic niches. The PGs that supported the growth of L. acidophilus were utilized poorly or not at all by other common HGM strains, underscoring the metabolic specialization of L. acidophilus. These findings highlight the role of human gut L. acidophilus and select lactobacilli in the bioconversion of glycoconjugated phytochemicals, which is likely to have an important impact on the HGM and human host. IMPORTANCE Thousands of therapeutically active plant-derived compounds are widely present in berries, fruits, nuts, and beverages like tea and wine. The bioactivity and bioavailability of these compounds, which are typically glycosylated, are altered by microbial bioconversions in the human gut. Remarkably, little is known about the bioconversion of PGs by the gut microbial community, despite the significance of this metabolic facet to human health. Our work provides the first molecular insights into the metabolic routes of diet relevant and therapeutically active PGs by Lactobacillus acidophilus and related human gut lactobacilli. This taxonomic group is adept at metabolizing the glucoside moieties of select PG and externalizes their aglycones. The study highlights an important role of lactobacilli in the bioconversion of dietary PG and presents a framework from which to derive molecular insights into their metabolism by members of the human gut microbiota.Mia C. TheilmannYong Jun GohKristian Fog NielsenTodd R. KlaenhammerRodolphe BarrangouMaher Abou HachemAmerican Society for MicrobiologyarticleLactobacillusbeta-glucosidebioavailabilitygut microbiotaphytochemicalpolydatinMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Lactobacillus beta-glucoside bioavailability gut microbiota phytochemical polydatin Microbiology QR1-502
spellingShingle	Lactobacillus beta-glucoside bioavailability gut microbiota phytochemical polydatin Microbiology QR1-502 Mia C. Theilmann Yong Jun Goh Kristian Fog Nielsen Todd R. Klaenhammer Rodolphe Barrangou Maher Abou Hachem <italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
description	ABSTRACT Therapeutically active glycosylated phytochemicals are ubiquitous in the human diet. The human gut microbiota (HGM) modulates the bioactivities of these compounds, which consequently affect host physiology and microbiota composition. Despite a significant impact on human health, the key players and the underpinning mechanisms of this interplay remain uncharacterized. Here, we demonstrate the growth of Lactobacillus acidophilus on mono- and diglucosyl dietary plant glycosides (PGs) possessing small aromatic aglycones. Transcriptional analysis revealed the upregulation of host interaction genes and identified two loci that encode phosphotransferase system (PTS) transporters and phospho-β-glucosidases, which mediate the uptake and deglucosylation of these compounds, respectively. Inactivating these transport and hydrolysis genes abolished or severely reduced growth on PG, establishing the specificity of the loci to distinct groups of PGs. Following intracellular deglucosylation, the aglycones of PGs are externalized, rendering them available for absorption by the host or for further modification by other microbiota taxa. The PG utilization loci are conserved in L. acidophilus and closely related lactobacilli, in correlation with versatile growth on these compounds. Growth on the tested PG appeared more common among human gut lactobacilli than among counterparts from other ecologic niches. The PGs that supported the growth of L. acidophilus were utilized poorly or not at all by other common HGM strains, underscoring the metabolic specialization of L. acidophilus. These findings highlight the role of human gut L. acidophilus and select lactobacilli in the bioconversion of glycoconjugated phytochemicals, which is likely to have an important impact on the HGM and human host. IMPORTANCE Thousands of therapeutically active plant-derived compounds are widely present in berries, fruits, nuts, and beverages like tea and wine. The bioactivity and bioavailability of these compounds, which are typically glycosylated, are altered by microbial bioconversions in the human gut. Remarkably, little is known about the bioconversion of PGs by the gut microbial community, despite the significance of this metabolic facet to human health. Our work provides the first molecular insights into the metabolic routes of diet relevant and therapeutically active PGs by Lactobacillus acidophilus and related human gut lactobacilli. This taxonomic group is adept at metabolizing the glucoside moieties of select PG and externalizes their aglycones. The study highlights an important role of lactobacilli in the bioconversion of dietary PG and presents a framework from which to derive molecular insights into their metabolism by members of the human gut microbiota.
format	article
author	Mia C. Theilmann Yong Jun Goh Kristian Fog Nielsen Todd R. Klaenhammer Rodolphe Barrangou Maher Abou Hachem
author_facet	Mia C. Theilmann Yong Jun Goh Kristian Fog Nielsen Todd R. Klaenhammer Rodolphe Barrangou Maher Abou Hachem
author_sort	Mia C. Theilmann
title	<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
title_short	<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
title_full	<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
title_fullStr	<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
title_full_unstemmed	<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals
title_sort	<italic toggle="yes">lactobacillus acidophilus</italic> metabolizes dietary plant glucosides and externalizes their bioactive phytochemicals
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/c272d79e522f4bdca314091d9e187d49
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<italic toggle="yes">Lactobacillus acidophilus</italic> Metabolizes Dietary Plant Glucosides and Externalizes Their Bioactive Phytochemicals

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