<i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine

The mechanism behind how flavin mononucleotide (FMN)-producing bacteria attach to a host intestine remains unclear. In order to address this issue, this study isolated the Gram-positive bacteria <i>Lactobacillus plantarum</i> from Mongolian fermented Airag, named <i>L</i>. &l...

Full description

Bibliographic Details
Main Authors: Binderiya Ganzorig, Enkhbat Zayabaatar, Minh Tan Pham, Shinta Marito, Chun-Ming Huang, Yu-Hsiang Lee
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Biomedicines
Subjects:
Online Access:https://www.mdpi.com/2227-9059/11/3/677
_version_ 1797613322959323136
author Binderiya Ganzorig
Enkhbat Zayabaatar
Minh Tan Pham
Shinta Marito
Chun-Ming Huang
Yu-Hsiang Lee
author_facet Binderiya Ganzorig
Enkhbat Zayabaatar
Minh Tan Pham
Shinta Marito
Chun-Ming Huang
Yu-Hsiang Lee
author_sort Binderiya Ganzorig
collection DOAJ
description The mechanism behind how flavin mononucleotide (FMN)-producing bacteria attach to a host intestine remains unclear. In order to address this issue, this study isolated the Gram-positive bacteria <i>Lactobacillus plantarum</i> from Mongolian fermented Airag, named <i>L</i>. <i>plantarum</i> MA. These bacteria were further employed as the model microbes, and their electrogenic properties were first identified by their significant expression of type II NADH-quinone oxidoreductase. This study also demonstrated that the electrical activity of <i>L. plantarum</i> MA can be conducted through flavin mononucleotide (FMN)-based extracellular electron transfer, which is highly dependent on the presence of a carbon source in the medium. Our data show that approximately 15 µM of FMN, one of the key electron donors for the generation of electricity, can be produced from <i>L. plantarum</i> MA, as they were cultured in the presence of lactulose for 24 h. We further demonstrated that the electrical activity of <i>L. plantarum</i> MA can promote microbial adhesion and can thus enhance the colonization effectiveness of Caco-2 cells and mouse cecum. Such enhanced adhesiveness was attributed to the increased expression of type I collagens in the intestinal epithelium after treatment with <i>L. plantarum</i> MA. This study reveals the mechanism behind the electrogenic activity of <i>L. plantarum</i> MA and shows how the bacteria utilize electricity to modulate the protein expression of gut tissue for an enhanced adhesion process.
first_indexed 2024-03-11T06:54:15Z
format Article
id doaj.art-297ab275df6e40f4910ff38e22111195
institution Directory Open Access Journal
issn 2227-9059
language English
last_indexed 2024-03-11T06:54:15Z
publishDate 2023-02-01
publisher MDPI AG
record_format Article
series Biomedicines
spelling doaj.art-297ab275df6e40f4910ff38e221111952023-11-17T09:43:59ZengMDPI AGBiomedicines2227-90592023-02-0111367710.3390/biomedicines11030677<i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to IntestineBinderiya Ganzorig0Enkhbat Zayabaatar1Minh Tan Pham2Shinta Marito3Chun-Ming Huang4Yu-Hsiang Lee5Department of Biomedical Sciences and Engineering, National Central University, Taoyuan City 320317, TaiwanDepartment of Biomedical Sciences and Engineering, National Central University, Taoyuan City 320317, TaiwanFaculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City 700000, VietnamDepartment of Biomedical Sciences and Engineering, National Central University, Taoyuan City 320317, TaiwanDepartment of Biomedical Sciences and Engineering, National Central University, Taoyuan City 320317, TaiwanDepartment of Biomedical Sciences and Engineering, National Central University, Taoyuan City 320317, TaiwanThe mechanism behind how flavin mononucleotide (FMN)-producing bacteria attach to a host intestine remains unclear. In order to address this issue, this study isolated the Gram-positive bacteria <i>Lactobacillus plantarum</i> from Mongolian fermented Airag, named <i>L</i>. <i>plantarum</i> MA. These bacteria were further employed as the model microbes, and their electrogenic properties were first identified by their significant expression of type II NADH-quinone oxidoreductase. This study also demonstrated that the electrical activity of <i>L. plantarum</i> MA can be conducted through flavin mononucleotide (FMN)-based extracellular electron transfer, which is highly dependent on the presence of a carbon source in the medium. Our data show that approximately 15 µM of FMN, one of the key electron donors for the generation of electricity, can be produced from <i>L. plantarum</i> MA, as they were cultured in the presence of lactulose for 24 h. We further demonstrated that the electrical activity of <i>L. plantarum</i> MA can promote microbial adhesion and can thus enhance the colonization effectiveness of Caco-2 cells and mouse cecum. Such enhanced adhesiveness was attributed to the increased expression of type I collagens in the intestinal epithelium after treatment with <i>L. plantarum</i> MA. This study reveals the mechanism behind the electrogenic activity of <i>L. plantarum</i> MA and shows how the bacteria utilize electricity to modulate the protein expression of gut tissue for an enhanced adhesion process.https://www.mdpi.com/2227-9059/11/3/677<i>L. plantarum</i>electricitycarbon sourceflavin mononucleotideextracellular electron transfermicrobial adhesion
spellingShingle Binderiya Ganzorig
Enkhbat Zayabaatar
Minh Tan Pham
Shinta Marito
Chun-Ming Huang
Yu-Hsiang Lee
<i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
Biomedicines
<i>L. plantarum</i>
electricity
carbon source
flavin mononucleotide
extracellular electron transfer
microbial adhesion
title <i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
title_full <i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
title_fullStr <i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
title_full_unstemmed <i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
title_short <i>Lactobacillus plantarum</i> Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine
title_sort i lactobacillus plantarum i generate electricity through flavin mononucleotide mediated extracellular electron transfer to upregulate epithelial type i collagen expression and thereby promote microbial adhesion to intestine
topic <i>L. plantarum</i>
electricity
carbon source
flavin mononucleotide
extracellular electron transfer
microbial adhesion
url https://www.mdpi.com/2227-9059/11/3/677
work_keys_str_mv AT binderiyaganzorig ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine
AT enkhbatzayabaatar ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine
AT minhtanpham ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine
AT shintamarito ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine
AT chunminghuang ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine
AT yuhsianglee ilactobacillusplantarumigenerateelectricitythroughflavinmononucleotidemediatedextracellularelectrontransfertoupregulateepithelialtypeicollagenexpressionandtherebypromotemicrobialadhesiontointestine