In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors

ABSTRACTFecal microbiota transplantation (FMT) is used routinely to treat recurrent Clostridioides difficile infection (rCDI) and investigated as a treatment for numerous conditions associated with gut microbiota alterations. Metagenomic analyses have indicated that recipient colonization by donor b...

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Main Authors: Aki Ronkainen, Imran Khan, Eva Krzyżewska-Dudek, Kaisa Hiippala, Tobias L. Freitag, Reetta Satokari
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2023.2229944
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author Aki Ronkainen
Imran Khan
Eva Krzyżewska-Dudek
Kaisa Hiippala
Tobias L. Freitag
Reetta Satokari
author_facet Aki Ronkainen
Imran Khan
Eva Krzyżewska-Dudek
Kaisa Hiippala
Tobias L. Freitag
Reetta Satokari
author_sort Aki Ronkainen
collection DOAJ
description ABSTRACTFecal microbiota transplantation (FMT) is used routinely to treat recurrent Clostridioides difficile infection (rCDI) and investigated as a treatment for numerous conditions associated with gut microbiota alterations. Metagenomic analyses have indicated that recipient colonization by donor bacteria may be associated with favorable clinical outcomes. Bifidobacteria are abundant gut commensals associated with health. We have previously demonstrated that Bifidobacterium strains transferred in FMT can colonize recipients in long term, at least for a year, and recovered such strains by cultivation. This study addressed in vitro adhesion and pilus gene expression of long-term colonizing Bifidobacterium strains from FMT donors as well as in vivo colonization and capability to ameliorate antibiotic-induced microbiota disturbance. RNA-Seq differential gene expression analysis showed that the strongly adherent B. longum strains DY_pv11 and DX_pv23 expressed tight adherence and sortase-dependent pilus genes, respectively. Two B. longum strains, adherent DX_pv23 and poorly adhering DX_pv18, were selected to address in vivo colonization and efficacy to restore antibiotic-disturbed microbiota in C57BL/6 murine model. DX_pv23 colonized mice transiently with a rate comparable to that of the B. animalis BB-12 used as a reference. Although long-term colonization was not observed with any of the three strains, 16S rRNA gene profiling revealed that oral administration of DX_pv23 enhanced the recovery of antibiotic-disturbed microbiota to the original configuration significantly better than the other strains. The findings suggest that selected strains from FMT donors, such as DX_pv23 in this study, may have therapeutic potential by in vitro expression of colonization factors and boosting endogenous gut microbiota.
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spelling doaj.art-001ee73a757e438abce179b335e5686f2024-03-28T22:38:21ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2229944In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donorsAki Ronkainen0Imran Khan1Eva Krzyżewska-Dudek2Kaisa Hiippala3Tobias L. Freitag4Reetta Satokari5Human Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandTranslational Immunology Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandTranslational Immunology Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandABSTRACTFecal microbiota transplantation (FMT) is used routinely to treat recurrent Clostridioides difficile infection (rCDI) and investigated as a treatment for numerous conditions associated with gut microbiota alterations. Metagenomic analyses have indicated that recipient colonization by donor bacteria may be associated with favorable clinical outcomes. Bifidobacteria are abundant gut commensals associated with health. We have previously demonstrated that Bifidobacterium strains transferred in FMT can colonize recipients in long term, at least for a year, and recovered such strains by cultivation. This study addressed in vitro adhesion and pilus gene expression of long-term colonizing Bifidobacterium strains from FMT donors as well as in vivo colonization and capability to ameliorate antibiotic-induced microbiota disturbance. RNA-Seq differential gene expression analysis showed that the strongly adherent B. longum strains DY_pv11 and DX_pv23 expressed tight adherence and sortase-dependent pilus genes, respectively. Two B. longum strains, adherent DX_pv23 and poorly adhering DX_pv18, were selected to address in vivo colonization and efficacy to restore antibiotic-disturbed microbiota in C57BL/6 murine model. DX_pv23 colonized mice transiently with a rate comparable to that of the B. animalis BB-12 used as a reference. Although long-term colonization was not observed with any of the three strains, 16S rRNA gene profiling revealed that oral administration of DX_pv23 enhanced the recovery of antibiotic-disturbed microbiota to the original configuration significantly better than the other strains. The findings suggest that selected strains from FMT donors, such as DX_pv23 in this study, may have therapeutic potential by in vitro expression of colonization factors and boosting endogenous gut microbiota.https://www.tandfonline.com/doi/10.1080/19490976.2023.2229944Bacteriotherapydysbiosisfecal microbiota transplantationgut microbiotanext-generation probiotics
spellingShingle Aki Ronkainen
Imran Khan
Eva Krzyżewska-Dudek
Kaisa Hiippala
Tobias L. Freitag
Reetta Satokari
In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
Gut Microbes
Bacteriotherapy
dysbiosis
fecal microbiota transplantation
gut microbiota
next-generation probiotics
title In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
title_full In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
title_fullStr In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
title_full_unstemmed In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
title_short In vitro adhesion, pilus expression, and in vivo amelioration of antibiotic-induced microbiota disturbance by Bifidobacterium spp. strains from fecal donors
title_sort in vitro adhesion pilus expression and in vivo amelioration of antibiotic induced microbiota disturbance by bifidobacterium spp strains from fecal donors
topic Bacteriotherapy
dysbiosis
fecal microbiota transplantation
gut microbiota
next-generation probiotics
url https://www.tandfonline.com/doi/10.1080/19490976.2023.2229944
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