Cargando…

Microbiome of root vegetables—a source of gluten-degrading bacteria

ABSTRACT: Gluten is a cereal protein that is incompletely digested by human proteolytic enzymes that create immunogenic peptides that accumulate in the gastrointestinal tract (GIT). Although both environmental and human bacteria have been shown to expedite gluten hydrolysis, gluten intolerance is a...

Descripción completa

Detalles Bibliográficos
Autores principales: Kõiv, Viia, Adamberg, Kaarel, Adamberg, Signe, Sumeri, Ingrid, Kasvandik, Sergo, Kisand, Veljo, Maiväli, Ülo, Tenson, Tanel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502452/
https://www.ncbi.nlm.nih.gov/pubmed/32875365
http://dx.doi.org/10.1007/s00253-020-10852-0
_version_ 1783584228252844032
author Kõiv, Viia
Adamberg, Kaarel
Adamberg, Signe
Sumeri, Ingrid
Kasvandik, Sergo
Kisand, Veljo
Maiväli, Ülo
Tenson, Tanel
author_facet Kõiv, Viia
Adamberg, Kaarel
Adamberg, Signe
Sumeri, Ingrid
Kasvandik, Sergo
Kisand, Veljo
Maiväli, Ülo
Tenson, Tanel
author_sort Kõiv, Viia
collection PubMed
description ABSTRACT: Gluten is a cereal protein that is incompletely digested by human proteolytic enzymes that create immunogenic peptides that accumulate in the gastrointestinal tract (GIT). Although both environmental and human bacteria have been shown to expedite gluten hydrolysis, gluten intolerance is a growing concern. Here we hypothesize that together with food, we acquire environmental bacteria that could impact our GIT with gluten-degrading bacteria. Using in vitro gastrointestinal simulation conditions, we evaluated the capacity of endophytic bacteria that inhabit root vegetables, potato (Solanum tuberosum), carrot (Daucus sativus), beet (Beta vulgaris), and topinambur (Jerusalem artichoke) (Helianthus tuberosus), to resist these conditions and degrade gluten. By 16S rDNA sequencing, we discovered that bacteria from the families Enterobacteriaceae, Bacillaceae, and Clostridiaceae most effectively multiply in conditions similar to the human GIT (microoxic conditions, 37 °C) while utilizing vegetable material and gluten as nutrients. Additionally, we used stomach simulation (1 h, pH 3) and intestinal simulation (1 h, bile salts 0.4%) treatments. The bacteria that survived this treatment retained the ability to degrade gluten epitopes but at lower levels. Four bacterial strains belonging to species Bacillus pumilus, Clostridium subterminale, and Clostridium sporogenes isolated from vegetable roots produced proteases with postproline cleaving activity that successfully neutralized the toxic immunogenic epitopes. KEY POINTS: • Bacteria from root vegetables can degrade gluten. • Some of these bacteria can resist conditions mimicking gastrointestinal tract. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s00253-020-10852-0) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-7502452
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Springer Berlin Heidelberg
record_format MEDLINE/PubMed
spelling pubmed-75024522020-10-05 Microbiome of root vegetables—a source of gluten-degrading bacteria Kõiv, Viia Adamberg, Kaarel Adamberg, Signe Sumeri, Ingrid Kasvandik, Sergo Kisand, Veljo Maiväli, Ülo Tenson, Tanel Appl Microbiol Biotechnol Applied Microbial and Cell Physiology ABSTRACT: Gluten is a cereal protein that is incompletely digested by human proteolytic enzymes that create immunogenic peptides that accumulate in the gastrointestinal tract (GIT). Although both environmental and human bacteria have been shown to expedite gluten hydrolysis, gluten intolerance is a growing concern. Here we hypothesize that together with food, we acquire environmental bacteria that could impact our GIT with gluten-degrading bacteria. Using in vitro gastrointestinal simulation conditions, we evaluated the capacity of endophytic bacteria that inhabit root vegetables, potato (Solanum tuberosum), carrot (Daucus sativus), beet (Beta vulgaris), and topinambur (Jerusalem artichoke) (Helianthus tuberosus), to resist these conditions and degrade gluten. By 16S rDNA sequencing, we discovered that bacteria from the families Enterobacteriaceae, Bacillaceae, and Clostridiaceae most effectively multiply in conditions similar to the human GIT (microoxic conditions, 37 °C) while utilizing vegetable material and gluten as nutrients. Additionally, we used stomach simulation (1 h, pH 3) and intestinal simulation (1 h, bile salts 0.4%) treatments. The bacteria that survived this treatment retained the ability to degrade gluten epitopes but at lower levels. Four bacterial strains belonging to species Bacillus pumilus, Clostridium subterminale, and Clostridium sporogenes isolated from vegetable roots produced proteases with postproline cleaving activity that successfully neutralized the toxic immunogenic epitopes. KEY POINTS: • Bacteria from root vegetables can degrade gluten. • Some of these bacteria can resist conditions mimicking gastrointestinal tract. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s00253-020-10852-0) contains supplementary material, which is available to authorized users. Springer Berlin Heidelberg 2020-09-02 2020 /pmc/articles/PMC7502452/ /pubmed/32875365 http://dx.doi.org/10.1007/s00253-020-10852-0 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Applied Microbial and Cell Physiology
Kõiv, Viia
Adamberg, Kaarel
Adamberg, Signe
Sumeri, Ingrid
Kasvandik, Sergo
Kisand, Veljo
Maiväli, Ülo
Tenson, Tanel
Microbiome of root vegetables—a source of gluten-degrading bacteria
title Microbiome of root vegetables—a source of gluten-degrading bacteria
title_full Microbiome of root vegetables—a source of gluten-degrading bacteria
title_fullStr Microbiome of root vegetables—a source of gluten-degrading bacteria
title_full_unstemmed Microbiome of root vegetables—a source of gluten-degrading bacteria
title_short Microbiome of root vegetables—a source of gluten-degrading bacteria
title_sort microbiome of root vegetables—a source of gluten-degrading bacteria
topic Applied Microbial and Cell Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502452/
https://www.ncbi.nlm.nih.gov/pubmed/32875365
http://dx.doi.org/10.1007/s00253-020-10852-0
work_keys_str_mv AT koivviia microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT adambergkaarel microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT adambergsigne microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT sumeriingrid microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT kasvandiksergo microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT kisandveljo microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT maivaliulo microbiomeofrootvegetablesasourceofglutendegradingbacteria
AT tensontanel microbiomeofrootvegetablesasourceofglutendegradingbacteria