Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized

Bacteria-host interactions are mediated by different microbial associated molecular patterns which are most often surface structures such as, among others, exopolysaccharides (EPSs). In this work, the capability of two isogenic EPS-producing Bifidobacterium animalis subsp. lactis strains to modulate...

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Main Authors: Carlos Sabater, Natalia Molinero-García, Nuria Castro-Bravo, Patricia Diez-Echave, Laura Hidalgo-García, Susana Delgado, Borja Sánchez, Julio Gálvez, Abelardo Margolles, Patricia Ruas-Madiedo
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.601233/full
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author Carlos Sabater
Carlos Sabater
Natalia Molinero-García
Natalia Molinero-García
Nuria Castro-Bravo
Nuria Castro-Bravo
Patricia Diez-Echave
Patricia Diez-Echave
Laura Hidalgo-García
Laura Hidalgo-García
Susana Delgado
Susana Delgado
Borja Sánchez
Borja Sánchez
Julio Gálvez
Julio Gálvez
Abelardo Margolles
Abelardo Margolles
Patricia Ruas-Madiedo
Patricia Ruas-Madiedo
author_facet Carlos Sabater
Carlos Sabater
Natalia Molinero-García
Natalia Molinero-García
Nuria Castro-Bravo
Nuria Castro-Bravo
Patricia Diez-Echave
Patricia Diez-Echave
Laura Hidalgo-García
Laura Hidalgo-García
Susana Delgado
Susana Delgado
Borja Sánchez
Borja Sánchez
Julio Gálvez
Julio Gálvez
Abelardo Margolles
Abelardo Margolles
Patricia Ruas-Madiedo
Patricia Ruas-Madiedo
author_sort Carlos Sabater
collection DOAJ
description Bacteria-host interactions are mediated by different microbial associated molecular patterns which are most often surface structures such as, among others, exopolysaccharides (EPSs). In this work, the capability of two isogenic EPS-producing Bifidobacterium animalis subsp. lactis strains to modulate the gut microbiota of healthy mice, was assessed. Each strain produces a different type of polymer; the ropy strain S89L synthesized a rhamnose-rich, high-molecular weight EPS in highest abundance than the non-ropy DMS10140 one. BALB/c mice were orally fed for 10 days with milk-bifidobacterial suspensions and followed afterward for 7 post-intervention days (wash-out period). The colonic content of mice was collected in several sampling points to perform a metataxonomic analysis. In addition, the influence of specific microbial clades, apparently stimulated by the ropy and non-ropy strains, on mouse plasmatic cytokine levels was investigated through hierarchical association testing. Analysis of 16S rRNA gene sequences showed that the abundance of Firmicutes phylum significantly increased 7 days after cessing the treatment with both strains. The relative abundance of Alloprevotella genus also rose, but after shorter post-treatment times (3 days for both DMS10140 and S89L strains). Some bacterial clades were specifically modulated by one or another strain. As such, the non-ropy DMS10140 strain exerted a significant influence on Intestinomonas genus, which increased after 4 post-administration days. On the other hand, feeding with the ropy strain S89L led to an increase in sequences of Faecalibaculum genus at 4 post-treatment days, while the abundance of Erysipelotrichaceae and Lactobacillaceae families increased for prolonged times. Association testing revealed that several lactobacilli and bifidobacterial significantly stimulated by ropy S89L strain were positively associated with the levels of certain cytokines, including IL-5 and IL-27. These results highlight relevant changes in mice gut microbiota produced after administration of the ropy S89L strain that were associated to a potential immune modulation effect.
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spelling doaj.art-ba594f5f77ff4ab69a7e3cf7b591d5ff2022-12-21T20:19:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-11-011110.3389/fmicb.2020.601233601233Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer SynthesizedCarlos Sabater0Carlos Sabater1Natalia Molinero-García2Natalia Molinero-García3Nuria Castro-Bravo4Nuria Castro-Bravo5Patricia Diez-Echave6Patricia Diez-Echave7Laura Hidalgo-García8Laura Hidalgo-García9Susana Delgado10Susana Delgado11Borja Sánchez12Borja Sánchez13Julio Gálvez14Julio Gálvez15Abelardo Margolles16Abelardo Margolles17Patricia Ruas-Madiedo18Patricia Ruas-Madiedo19Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainCIBER-EHD, Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, SpainInstituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, SpainCIBER-EHD, Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, SpainInstituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainCIBER-EHD, Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, SpainInstituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainDepartment of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias – Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, SpainMicrohealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, SpainBacteria-host interactions are mediated by different microbial associated molecular patterns which are most often surface structures such as, among others, exopolysaccharides (EPSs). In this work, the capability of two isogenic EPS-producing Bifidobacterium animalis subsp. lactis strains to modulate the gut microbiota of healthy mice, was assessed. Each strain produces a different type of polymer; the ropy strain S89L synthesized a rhamnose-rich, high-molecular weight EPS in highest abundance than the non-ropy DMS10140 one. BALB/c mice were orally fed for 10 days with milk-bifidobacterial suspensions and followed afterward for 7 post-intervention days (wash-out period). The colonic content of mice was collected in several sampling points to perform a metataxonomic analysis. In addition, the influence of specific microbial clades, apparently stimulated by the ropy and non-ropy strains, on mouse plasmatic cytokine levels was investigated through hierarchical association testing. Analysis of 16S rRNA gene sequences showed that the abundance of Firmicutes phylum significantly increased 7 days after cessing the treatment with both strains. The relative abundance of Alloprevotella genus also rose, but after shorter post-treatment times (3 days for both DMS10140 and S89L strains). Some bacterial clades were specifically modulated by one or another strain. As such, the non-ropy DMS10140 strain exerted a significant influence on Intestinomonas genus, which increased after 4 post-administration days. On the other hand, feeding with the ropy strain S89L led to an increase in sequences of Faecalibaculum genus at 4 post-treatment days, while the abundance of Erysipelotrichaceae and Lactobacillaceae families increased for prolonged times. Association testing revealed that several lactobacilli and bifidobacterial significantly stimulated by ropy S89L strain were positively associated with the levels of certain cytokines, including IL-5 and IL-27. These results highlight relevant changes in mice gut microbiota produced after administration of the ropy S89L strain that were associated to a potential immune modulation effect.https://www.frontiersin.org/articles/10.3389/fmicb.2020.601233/fullexopolysaccharidebifidobacteriamicrobiotamicecytokineimmune response
spellingShingle Carlos Sabater
Carlos Sabater
Natalia Molinero-García
Natalia Molinero-García
Nuria Castro-Bravo
Nuria Castro-Bravo
Patricia Diez-Echave
Patricia Diez-Echave
Laura Hidalgo-García
Laura Hidalgo-García
Susana Delgado
Susana Delgado
Borja Sánchez
Borja Sánchez
Julio Gálvez
Julio Gálvez
Abelardo Margolles
Abelardo Margolles
Patricia Ruas-Madiedo
Patricia Ruas-Madiedo
Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
Frontiers in Microbiology
exopolysaccharide
bifidobacteria
microbiota
mice
cytokine
immune response
title Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
title_full Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
title_fullStr Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
title_full_unstemmed Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
title_short Exopolysaccharide Producing Bifidobacterium animalis subsp. lactis Strains Modify the Intestinal Microbiota and the Plasmatic Cytokine Levels of BALB/c Mice According to the Type of Polymer Synthesized
title_sort exopolysaccharide producing bifidobacterium animalis subsp lactis strains modify the intestinal microbiota and the plasmatic cytokine levels of balb c mice according to the type of polymer synthesized
topic exopolysaccharide
bifidobacteria
microbiota
mice
cytokine
immune response
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.601233/full
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