The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation

ABSTRACT Various Lactobacillus species have been reported to deconjugate bile acids in the gastrointestinal tract (GIT) through the action of bile salt hydrolase (BSH) proteins. This function contributes to altering the gut microbiota composition and bile metabolism and detoxification and to lowerin...

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Autores principales:	Sarah O’Flaherty, Alexandra Briner Crawley, Casey M. Theriot, Rodolphe Barrangou
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Lactobacillus bile acid bile salt hydrolase gastrointestinal tract niche penicillin V acylase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e232f21167694520af355720eab6b856
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spelling	oai:doaj.org-article:e232f21167694520af355720eab6b8562021-11-15T15:24:23ZThe <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation10.1128/mSphere.00140-182379-5042https://doaj.org/article/e232f21167694520af355720eab6b8562018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00140-18https://doaj.org/toc/2379-5042ABSTRACT Various Lactobacillus species have been reported to deconjugate bile acids in the gastrointestinal tract (GIT) through the action of bile salt hydrolase (BSH) proteins. This function contributes to altering the gut microbiota composition and bile metabolism and detoxification and to lowering cholesterol levels. Here, we investigated the Lactobacillus BSH repertoire across 170 sequenced species. We used hidden Markov models to distinguish between BSH and closely related penicillin-V acylase (PVA) proteins. Even though BSH and PVA proteins have very different target substrates, they share high sequence similarity and are often misannotated. We determined that 82/170 (48.24%) species encoded PVA proteins, 39/170 (22.94%) species encoded BSH proteins, and 8/170 (4.71%) species encoded both BSH and PVA proteins, while 57/170 (33.53%) species encoded neither. Mapping the occurrence of BSH-encoding species onto a phylogenetic tree revealed that BSH-encoding lactobacilli primarily adopt the vertebrate-adapted lifestyle but not the environmental or plant-associated subsets. Phylogenetic analysis of the BSH sequences revealed two distinct clades, several conserved motifs, and the presence of six previously reported active-site residues. These data will guide future mechanistic studies of BSH activity and contribute to the development and selection of BSH-encoding Lactobacillus strains with therapeutic potential. IMPORTANCE Bile acids play an integral role in shaping the gut microbiota and host physiology by regulating metabolic signaling, weight gain, and serum cholesterol and liver triglyceride levels. Given these important roles of bile acids, we investigated the presence of bile salt hydrolase (BSH) in Lactobacillus genomes representing 170 different species, determined strain- and species-specific patterns of occurrences, and expanded on the diversity of the BSH repertoire in this genus. While our data showed that 28% of Lactobacillus species encode BSH proteins, these species are associated mainly with vertebrate-adapted niches, demonstrating selective pressure on lactobacilli to evolve to adapt to specific environments. These new data will allow targeted selection of specific strains of lactobacilli and BSH proteins for future mechanistic studies to explore their therapeutic potential for treating metabolic disorders.Sarah O’FlahertyAlexandra Briner CrawleyCasey M. TheriotRodolphe BarrangouAmerican Society for MicrobiologyarticleLactobacillusbile acidbile salt hydrolasegastrointestinal tractnichepenicillin V acylaseMicrobiologyQR1-502ENmSphere, Vol 3, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Lactobacillus bile acid bile salt hydrolase gastrointestinal tract niche penicillin V acylase Microbiology QR1-502
spellingShingle	Lactobacillus bile acid bile salt hydrolase gastrointestinal tract niche penicillin V acylase Microbiology QR1-502 Sarah O’Flaherty Alexandra Briner Crawley Casey M. Theriot Rodolphe Barrangou The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
description	ABSTRACT Various Lactobacillus species have been reported to deconjugate bile acids in the gastrointestinal tract (GIT) through the action of bile salt hydrolase (BSH) proteins. This function contributes to altering the gut microbiota composition and bile metabolism and detoxification and to lowering cholesterol levels. Here, we investigated the Lactobacillus BSH repertoire across 170 sequenced species. We used hidden Markov models to distinguish between BSH and closely related penicillin-V acylase (PVA) proteins. Even though BSH and PVA proteins have very different target substrates, they share high sequence similarity and are often misannotated. We determined that 82/170 (48.24%) species encoded PVA proteins, 39/170 (22.94%) species encoded BSH proteins, and 8/170 (4.71%) species encoded both BSH and PVA proteins, while 57/170 (33.53%) species encoded neither. Mapping the occurrence of BSH-encoding species onto a phylogenetic tree revealed that BSH-encoding lactobacilli primarily adopt the vertebrate-adapted lifestyle but not the environmental or plant-associated subsets. Phylogenetic analysis of the BSH sequences revealed two distinct clades, several conserved motifs, and the presence of six previously reported active-site residues. These data will guide future mechanistic studies of BSH activity and contribute to the development and selection of BSH-encoding Lactobacillus strains with therapeutic potential. IMPORTANCE Bile acids play an integral role in shaping the gut microbiota and host physiology by regulating metabolic signaling, weight gain, and serum cholesterol and liver triglyceride levels. Given these important roles of bile acids, we investigated the presence of bile salt hydrolase (BSH) in Lactobacillus genomes representing 170 different species, determined strain- and species-specific patterns of occurrences, and expanded on the diversity of the BSH repertoire in this genus. While our data showed that 28% of Lactobacillus species encode BSH proteins, these species are associated mainly with vertebrate-adapted niches, demonstrating selective pressure on lactobacilli to evolve to adapt to specific environments. These new data will allow targeted selection of specific strains of lactobacilli and BSH proteins for future mechanistic studies to explore their therapeutic potential for treating metabolic disorders.
format	article
author	Sarah O’Flaherty Alexandra Briner Crawley Casey M. Theriot Rodolphe Barrangou
author_facet	Sarah O’Flaherty Alexandra Briner Crawley Casey M. Theriot Rodolphe Barrangou
author_sort	Sarah O’Flaherty
title	The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
title_short	The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
title_full	The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
title_fullStr	The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
title_full_unstemmed	The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation
title_sort	<italic toggle="yes">lactobacillus</italic> bile salt hydrolase repertoire reveals niche-specific adaptation
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/e232f21167694520af355720eab6b856
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The <italic toggle="yes">Lactobacillus</italic> Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation

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