Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice

Introduction: The gut microbiome is vital for providing resistance against colonized pathogenic bacteria. Recently, specific commensal species have become recognized as important mediators of host defense against microbial infection by a variety of mechanisms. Objectives: To examine the contribution...

Full description

Bibliographic Details
Main Authors: Jiaxiu Liu, Hongli Liu, Huanhuan Liu, Yue Teng, Ningbo Qin, Xiaomeng Ren, Xiaodong Xia
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:Journal of Advanced Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2090123223000905
_version_ 1827803666704236544
author Jiaxiu Liu
Hongli Liu
Huanhuan Liu
Yue Teng
Ningbo Qin
Xiaomeng Ren
Xiaodong Xia
author_facet Jiaxiu Liu
Hongli Liu
Huanhuan Liu
Yue Teng
Ningbo Qin
Xiaomeng Ren
Xiaodong Xia
author_sort Jiaxiu Liu
collection DOAJ
description Introduction: The gut microbiome is vital for providing resistance against colonized pathogenic bacteria. Recently, specific commensal species have become recognized as important mediators of host defense against microbial infection by a variety of mechanisms. Objectives: To examine the contribution of live and pasteurized A. muciniphila to defend against the intestinal pathogen Salmonella Typhimurium in a streptomycin-treated mouse model of infection. Methods: C57B6J mice were pretreated with phosphate-buffered saline (PBS), live Akkermansia muciniphila (AKK), and pasteurized A. muciniphila (pAKK) for two weeks, then mice were infected by S. Typhimurium SL 1344. 16S rRNA-based gut microbiota analysis was performed before and after infection. Bacterial counts in feces and tissues, histopathological analysis, gut barrier-related gene expression, and antimicrobial peptides were examined. Co-housing was performed to examine the role of microbiota in the change of susceptibility of mice to infection. Results: AKK and pAKK markedly decreased Salmonella fecal and systemic burdens and reduced inflammation during infection. Notably, further characterization of AKK and pAKK protective mechanisms revealed different candidate protective pathways. AKK promoted gut barrier gene expression and the secretion of antimicrobial peptides, and co-housing studies suggested that AKK-associated microbial community played a role in attenuating infection. Moreover, pAKK had a positive effect on NLRP3 in infected mice. We verified that pretreatment of pAKK could promote the expression of NLRP3, and enhance the antimicrobial activity of macrophage, likely through increasing the production of reactive oxygen (ROS), nitric oxide (NO), and inflammatory cytokines. Conclusion: Our study demonstrates that live or pasteurized A. muciniphila can be effective preventive measures for alleviating S. Typhimurium-induced disease, highlighting the potential of developing Akkermansia-based probiotics or postbiotics for the prevention of Salmonellosis.
first_indexed 2024-03-11T20:57:42Z
format Article
id doaj.art-65f00a42e92b4215937117e5fb0f775a
institution Directory Open Access Journal
issn 2090-1232
language English
last_indexed 2024-03-11T20:57:42Z
publishDate 2023-10-01
publisher Elsevier
record_format Article
series Journal of Advanced Research
spelling doaj.art-65f00a42e92b4215937117e5fb0f775a2023-09-30T04:54:23ZengElsevierJournal of Advanced Research2090-12322023-10-015289102Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in miceJiaxiu Liu0Hongli Liu1Huanhuan Liu2Yue Teng3Ningbo Qin4Xiaomeng Ren5Xiaodong Xia6National Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaNational Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaNational Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaNational Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaNational Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaNational Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaCorresponding author.; National Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian, Liaoning 116034, ChinaIntroduction: The gut microbiome is vital for providing resistance against colonized pathogenic bacteria. Recently, specific commensal species have become recognized as important mediators of host defense against microbial infection by a variety of mechanisms. Objectives: To examine the contribution of live and pasteurized A. muciniphila to defend against the intestinal pathogen Salmonella Typhimurium in a streptomycin-treated mouse model of infection. Methods: C57B6J mice were pretreated with phosphate-buffered saline (PBS), live Akkermansia muciniphila (AKK), and pasteurized A. muciniphila (pAKK) for two weeks, then mice were infected by S. Typhimurium SL 1344. 16S rRNA-based gut microbiota analysis was performed before and after infection. Bacterial counts in feces and tissues, histopathological analysis, gut barrier-related gene expression, and antimicrobial peptides were examined. Co-housing was performed to examine the role of microbiota in the change of susceptibility of mice to infection. Results: AKK and pAKK markedly decreased Salmonella fecal and systemic burdens and reduced inflammation during infection. Notably, further characterization of AKK and pAKK protective mechanisms revealed different candidate protective pathways. AKK promoted gut barrier gene expression and the secretion of antimicrobial peptides, and co-housing studies suggested that AKK-associated microbial community played a role in attenuating infection. Moreover, pAKK had a positive effect on NLRP3 in infected mice. We verified that pretreatment of pAKK could promote the expression of NLRP3, and enhance the antimicrobial activity of macrophage, likely through increasing the production of reactive oxygen (ROS), nitric oxide (NO), and inflammatory cytokines. Conclusion: Our study demonstrates that live or pasteurized A. muciniphila can be effective preventive measures for alleviating S. Typhimurium-induced disease, highlighting the potential of developing Akkermansia-based probiotics or postbiotics for the prevention of Salmonellosis.http://www.sciencedirect.com/science/article/pii/S2090123223000905Akkermansia muciniphilaSalmonella TyphimuriumGut microbiotaRegIII lectinsGut barriersInflammasomes
spellingShingle Jiaxiu Liu
Hongli Liu
Huanhuan Liu
Yue Teng
Ningbo Qin
Xiaomeng Ren
Xiaodong Xia
Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
Journal of Advanced Research
Akkermansia muciniphila
Salmonella Typhimurium
Gut microbiota
RegIII lectins
Gut barriers
Inflammasomes
title Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
title_full Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
title_fullStr Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
title_full_unstemmed Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
title_short Live and pasteurized Akkermansia muciniphila decrease susceptibility to Salmonella Typhimurium infection in mice
title_sort live and pasteurized akkermansia muciniphila decrease susceptibility to salmonella typhimurium infection in mice
topic Akkermansia muciniphila
Salmonella Typhimurium
Gut microbiota
RegIII lectins
Gut barriers
Inflammasomes
url http://www.sciencedirect.com/science/article/pii/S2090123223000905
work_keys_str_mv AT jiaxiuliu liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT hongliliu liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT huanhuanliu liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT yueteng liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT ningboqin liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT xiaomengren liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice
AT xiaodongxia liveandpasteurizedakkermansiamuciniphiladecreasesusceptibilitytosalmonellatyphimuriuminfectioninmice