Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection

Introduction: Galactooligosaccharides (GOS) are lactogenic prebiotics that exert health benefits by stimulating the growth of different Lactobacillus strains in the gastrointestinal (GI) tract. Objectives: This study aimed to investigate the mechanism of action of different GOS-enriched lactobacilli...

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Main Authors: Yujun Wu, Xiangyu Zhang, Xiaoyi Liu, Yi Li, Dandan Han, Yu Pi, Melanie A. Whitmore, Xingmiao Lu, Guolong Zhang, Jinkai Zheng, Junjun Wang
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Journal of Advanced Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S209012322300070X
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author Yujun Wu
Xiangyu Zhang
Xiaoyi Liu
Yi Li
Dandan Han
Yu Pi
Melanie A. Whitmore
Xingmiao Lu
Guolong Zhang
Jinkai Zheng
Junjun Wang
author_facet Yujun Wu
Xiangyu Zhang
Xiaoyi Liu
Yi Li
Dandan Han
Yu Pi
Melanie A. Whitmore
Xingmiao Lu
Guolong Zhang
Jinkai Zheng
Junjun Wang
author_sort Yujun Wu
collection DOAJ
description Introduction: Galactooligosaccharides (GOS) are lactogenic prebiotics that exert health benefits by stimulating the growth of different Lactobacillus strains in the gastrointestinal (GI) tract. Objectives: This study aimed to investigate the mechanism of action of different GOS-enriched lactobacilli in intestinal health. Methods: Piglets and mice were supplemented with GOS to identify specific enrichment of Lactobacillus. The protective effects of individual GOS-enriched lactobacilli were investigated in Salmonella-infected mice. Macrophage depletion and transcriptome analysis were further performed to assess the involvement of macrophages and the underlying mechanisms of individual lactobacilli. An in vitro cell co-culture system was also used to evaluate the anti-adhesive and anti-invasive activities of lactobacilli against Salmonella in epithelial cells. Results: GOS markedly increased the relative abundance of three lactobacilli including L. delbrueckii, L. johnsonii, and L. reuteri in both piglets and mice. Supplementation with GOS further alleviated Salmonella infection in mice. L. delbrueckii (ATCC®BAA 365™), but not L. johnsonii or L. reuteri, enhanced propionate production in the intestinal tract and ameliorated Salmonella-induced intestinal inflammation and barrier dysfunction by suppressing the JAK2-STAT3 signaling and M1 macrophage polarization. L. johnsonii (BNCC 186110), on the other hand, inhibited Salmonella adhesion and invasion of epithelial cells through competitive exclusion. However, L. reuteri (BNCC 186135) failed to protect mice against Salmonella infection. Conclusion: GOS-enriched lactobacilli show a differential role in protecting against Salmonella-induced intestinal barrier dysfunction and inflammation. Our results provide novel insights into the mechanism of action of GOS and individual Lactobacillus strains in the control and prevention of intestinal inflammatory disorders.
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spelling doaj.art-452a1520b0c4411e9b064cf9b29891b92024-01-31T05:42:54ZengElsevierJournal of Advanced Research2090-12322024-02-0156114Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infectionYujun Wu0Xiangyu Zhang1Xiaoyi Liu2Yi Li3Dandan Han4Yu Pi5Melanie A. Whitmore6Xingmiao Lu7Guolong Zhang8Jinkai Zheng9Junjun Wang10State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, ChinaDepartment of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USAInstitute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaDepartment of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USAInstitute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China; Corresponding author.Introduction: Galactooligosaccharides (GOS) are lactogenic prebiotics that exert health benefits by stimulating the growth of different Lactobacillus strains in the gastrointestinal (GI) tract. Objectives: This study aimed to investigate the mechanism of action of different GOS-enriched lactobacilli in intestinal health. Methods: Piglets and mice were supplemented with GOS to identify specific enrichment of Lactobacillus. The protective effects of individual GOS-enriched lactobacilli were investigated in Salmonella-infected mice. Macrophage depletion and transcriptome analysis were further performed to assess the involvement of macrophages and the underlying mechanisms of individual lactobacilli. An in vitro cell co-culture system was also used to evaluate the anti-adhesive and anti-invasive activities of lactobacilli against Salmonella in epithelial cells. Results: GOS markedly increased the relative abundance of three lactobacilli including L. delbrueckii, L. johnsonii, and L. reuteri in both piglets and mice. Supplementation with GOS further alleviated Salmonella infection in mice. L. delbrueckii (ATCC®BAA 365™), but not L. johnsonii or L. reuteri, enhanced propionate production in the intestinal tract and ameliorated Salmonella-induced intestinal inflammation and barrier dysfunction by suppressing the JAK2-STAT3 signaling and M1 macrophage polarization. L. johnsonii (BNCC 186110), on the other hand, inhibited Salmonella adhesion and invasion of epithelial cells through competitive exclusion. However, L. reuteri (BNCC 186135) failed to protect mice against Salmonella infection. Conclusion: GOS-enriched lactobacilli show a differential role in protecting against Salmonella-induced intestinal barrier dysfunction and inflammation. Our results provide novel insights into the mechanism of action of GOS and individual Lactobacillus strains in the control and prevention of intestinal inflammatory disorders.http://www.sciencedirect.com/science/article/pii/S209012322300070XGalactooligosaccharidesLactobacillusSalmonellaIntestinal inflammation
spellingShingle Yujun Wu
Xiangyu Zhang
Xiaoyi Liu
Yi Li
Dandan Han
Yu Pi
Melanie A. Whitmore
Xingmiao Lu
Guolong Zhang
Jinkai Zheng
Junjun Wang
Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
Journal of Advanced Research
Galactooligosaccharides
Lactobacillus
Salmonella
Intestinal inflammation
title Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
title_full Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
title_fullStr Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
title_full_unstemmed Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
title_short Strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during Salmonella infection
title_sort strain specificity of lactobacilli with promoted colonization by galactooligosaccharides administration in protecting intestinal barriers during salmonella infection
topic Galactooligosaccharides
Lactobacillus
Salmonella
Intestinal inflammation
url http://www.sciencedirect.com/science/article/pii/S209012322300070X
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