Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō

Spore-forming probiotic bacteria offer interesting properties as they have an intrinsic high stability, and when consumed, they are able to survive the adverse conditions encountered during the transit thorough the host gastrointestinal (GI) tract. A traditional healthy food, nattō, exists in Japan...

Full description

Bibliographic Details
Main Authors: Cecilia Leñini, Facundo Rodriguez Ayala, Anibal Juan Goñi, Liliana Rateni, Akira Nakamura, Roberto Ricardo Grau
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1253480/full
_version_ 1797670977417510912
author Cecilia Leñini
Facundo Rodriguez Ayala
Anibal Juan Goñi
Liliana Rateni
Akira Nakamura
Roberto Ricardo Grau
author_facet Cecilia Leñini
Facundo Rodriguez Ayala
Anibal Juan Goñi
Liliana Rateni
Akira Nakamura
Roberto Ricardo Grau
author_sort Cecilia Leñini
collection DOAJ
description Spore-forming probiotic bacteria offer interesting properties as they have an intrinsic high stability, and when consumed, they are able to survive the adverse conditions encountered during the transit thorough the host gastrointestinal (GI) tract. A traditional healthy food, nattō, exists in Japan consisting of soy fermented by the spore-forming bacterium Bacillus subtilis natto. The consumption of nattō is linked to many beneficial health effects, including the prevention of high blood pressure, osteoporosis, and cardiovascular-associated disease. We hypothesize that the bacterium B. subtilis natto plays a key role in the beneficial effects of nattō for humans. Here, we present the isolation of B. subtilis DG101 from nattō and its characterization as a novel spore-forming probiotic strain for human consumption. B. subtilis DG101 was non-hemolytic and showed high tolerance to lysozyme, low pH, bile salts, and a strong adherence ability to extracellular matrix proteins (i.e., fibronectin and collagen), demonstrating its potential application for competitive exclusion of pathogens. B. subtilis DG101 forms robust liquid and solid biofilms and expresses several extracellular enzymes with activity against food diet-associated macromolecules (i.e., proteins, lipids, and polysaccharides) that would be important to improve food diet digestion by the host. B. subtilis DG101 was able to grow in the presence of toxic metals (i.e., chromium, cadmium, and arsenic) and decreased their bioavailability, a feature that points to this probiotic as an interesting agent for bioremediation in cases of food and water poisoning with metals. In addition, B. subtilis DG101 was sensitive to antibiotics commonly used to treat infections in medical settings, and at the same time, it showed a potent antimicrobial effect against pathogenic bacteria and fungi. In mammalians (i.e., rats), B. subtilis DG101 colonized the GI tract, and improved the lipid and protein serum homeostasis of animals fed on the base of a normal- or a deficient-diet regime (dietary restriction). In the animal model for longevity studies, Caenorhabditis elegans, B. subtilis DG101 significantly increased the animal lifespan and prevented its age-related behavioral decay. Overall, these results demonstrate that B. subtilis DG101 is the key component of nattō with interesting probiotic properties to improve and protect human health.
first_indexed 2024-03-11T21:08:38Z
format Article
id doaj.art-3c6a2c61d50c46a98cd9949a6996da15
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-03-11T21:08:38Z
publishDate 2023-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-3c6a2c61d50c46a98cd9949a6996da152023-09-29T08:17:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12534801253480Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattōCecilia Leñini0Facundo Rodriguez Ayala1Anibal Juan Goñi2Liliana Rateni3Akira Nakamura4Roberto Ricardo Grau5Departamento de Microbiología, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, ArgentinaDepartamento de Microbiología, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, ArgentinaDepartamento de Microbiología, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, ArgentinaDepartamento de Microbiología, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, ArgentinaFaculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanDepartamento de Microbiología, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, ArgentinaSpore-forming probiotic bacteria offer interesting properties as they have an intrinsic high stability, and when consumed, they are able to survive the adverse conditions encountered during the transit thorough the host gastrointestinal (GI) tract. A traditional healthy food, nattō, exists in Japan consisting of soy fermented by the spore-forming bacterium Bacillus subtilis natto. The consumption of nattō is linked to many beneficial health effects, including the prevention of high blood pressure, osteoporosis, and cardiovascular-associated disease. We hypothesize that the bacterium B. subtilis natto plays a key role in the beneficial effects of nattō for humans. Here, we present the isolation of B. subtilis DG101 from nattō and its characterization as a novel spore-forming probiotic strain for human consumption. B. subtilis DG101 was non-hemolytic and showed high tolerance to lysozyme, low pH, bile salts, and a strong adherence ability to extracellular matrix proteins (i.e., fibronectin and collagen), demonstrating its potential application for competitive exclusion of pathogens. B. subtilis DG101 forms robust liquid and solid biofilms and expresses several extracellular enzymes with activity against food diet-associated macromolecules (i.e., proteins, lipids, and polysaccharides) that would be important to improve food diet digestion by the host. B. subtilis DG101 was able to grow in the presence of toxic metals (i.e., chromium, cadmium, and arsenic) and decreased their bioavailability, a feature that points to this probiotic as an interesting agent for bioremediation in cases of food and water poisoning with metals. In addition, B. subtilis DG101 was sensitive to antibiotics commonly used to treat infections in medical settings, and at the same time, it showed a potent antimicrobial effect against pathogenic bacteria and fungi. In mammalians (i.e., rats), B. subtilis DG101 colonized the GI tract, and improved the lipid and protein serum homeostasis of animals fed on the base of a normal- or a deficient-diet regime (dietary restriction). In the animal model for longevity studies, Caenorhabditis elegans, B. subtilis DG101 significantly increased the animal lifespan and prevented its age-related behavioral decay. Overall, these results demonstrate that B. subtilis DG101 is the key component of nattō with interesting probiotic properties to improve and protect human health.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1253480/fullprobioticsfermented soybeannattōBacillus subtilis DG101beneficial biofilmsmetal bioremediation
spellingShingle Cecilia Leñini
Facundo Rodriguez Ayala
Anibal Juan Goñi
Liliana Rateni
Akira Nakamura
Roberto Ricardo Grau
Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
Frontiers in Microbiology
probiotics
fermented soybean
nattō
Bacillus subtilis DG101
beneficial biofilms
metal bioremediation
title Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
title_full Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
title_fullStr Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
title_full_unstemmed Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
title_short Probiotic properties of Bacillus subtilis DG101 isolated from the traditional Japanese fermented food nattō
title_sort probiotic properties of bacillus subtilis dg101 isolated from the traditional japanese fermented food natto
topic probiotics
fermented soybean
nattō
Bacillus subtilis DG101
beneficial biofilms
metal bioremediation
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1253480/full
work_keys_str_mv AT cecilialenini probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto
AT facundorodriguezayala probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto
AT anibaljuangoni probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto
AT lilianarateni probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto
AT akiranakamura probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto
AT robertoricardograu probioticpropertiesofbacillussubtilisdg101isolatedfromthetraditionaljapanesefermentedfoodnatto