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Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses

Alginate oligosaccharides (AOS), extracted from marine brown algae, are a common functional feed additive; however, it remains unclear whether they modulate the gut microbiota and microbial metabolites. The response of Salmonella enterica serovar Typhimurium, a common poultry pathogen, to AOS fermen...

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Autores principales: Cheng, Jiaying, Xiao, Mengshi, Ren, Xinmiao, Secundo, Francesco, Yu, Ying, Nan, Shihao, Chen, Weimiao, Zhu, Changliang, Kong, Qing, Huang, Youtao, Fu, Xiaodan, Mou, Haijin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Nature Singapore 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10232696/
https://www.ncbi.nlm.nih.gov/pubmed/37275545
http://dx.doi.org/10.1007/s42995-023-00176-z
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author Cheng, Jiaying
Xiao, Mengshi
Ren, Xinmiao
Secundo, Francesco
Yu, Ying
Nan, Shihao
Chen, Weimiao
Zhu, Changliang
Kong, Qing
Huang, Youtao
Fu, Xiaodan
Mou, Haijin
author_facet Cheng, Jiaying
Xiao, Mengshi
Ren, Xinmiao
Secundo, Francesco
Yu, Ying
Nan, Shihao
Chen, Weimiao
Zhu, Changliang
Kong, Qing
Huang, Youtao
Fu, Xiaodan
Mou, Haijin
author_sort Cheng, Jiaying
collection PubMed
description Alginate oligosaccharides (AOS), extracted from marine brown algae, are a common functional feed additive; however, it remains unclear whether they modulate the gut microbiota and microbial metabolites. The response of Salmonella enterica serovar Typhimurium, a common poultry pathogen, to AOS fermented with chicken fecal inocula was investigated using metabolomic and transcriptomic analyses. Single-strain cultivation tests showed that AOS did not directly inhibit the growth of S. Typhimurium. However, when AOS were fermented by chicken fecal microbiota, the supernatant of fermented AOS (F-AOS) exhibited remarkable antibacterial activity against S. Typhimurium, decreasing the abundance ratio of S. Typhimurium in the fecal microbiota from 18.94 to 2.94%. Transcriptomic analyses showed that the 855 differentially expressed genes induced by F-AOS were mainly enriched in porphyrin and chlorophyll metabolism, oxidative phosphorylation, and Salmonella infection-related pathways. RT-qPCR confirmed that F-AOS downregulated key genes involved in flagellar assembly and the type III secretory system of S. Typhimurium, indicating metabolites in F-AOS can influence the growth and metabolism of S. Typhimurium. Metabolomic analyses showed that 205 microbial metabolites were significantly altered in F-AOS. Among them, the increase in indolelactic acid and 3-indolepropionic acid levels were further confirmed using HPLC. This study provides a new perspective for the application of AOS as a feed additive against pathogenic intestinal bacteria. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s42995-023-00176-z.
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spelling pubmed-102326962023-06-02 Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses Cheng, Jiaying Xiao, Mengshi Ren, Xinmiao Secundo, Francesco Yu, Ying Nan, Shihao Chen, Weimiao Zhu, Changliang Kong, Qing Huang, Youtao Fu, Xiaodan Mou, Haijin Mar Life Sci Technol Research Paper Alginate oligosaccharides (AOS), extracted from marine brown algae, are a common functional feed additive; however, it remains unclear whether they modulate the gut microbiota and microbial metabolites. The response of Salmonella enterica serovar Typhimurium, a common poultry pathogen, to AOS fermented with chicken fecal inocula was investigated using metabolomic and transcriptomic analyses. Single-strain cultivation tests showed that AOS did not directly inhibit the growth of S. Typhimurium. However, when AOS were fermented by chicken fecal microbiota, the supernatant of fermented AOS (F-AOS) exhibited remarkable antibacterial activity against S. Typhimurium, decreasing the abundance ratio of S. Typhimurium in the fecal microbiota from 18.94 to 2.94%. Transcriptomic analyses showed that the 855 differentially expressed genes induced by F-AOS were mainly enriched in porphyrin and chlorophyll metabolism, oxidative phosphorylation, and Salmonella infection-related pathways. RT-qPCR confirmed that F-AOS downregulated key genes involved in flagellar assembly and the type III secretory system of S. Typhimurium, indicating metabolites in F-AOS can influence the growth and metabolism of S. Typhimurium. Metabolomic analyses showed that 205 microbial metabolites were significantly altered in F-AOS. Among them, the increase in indolelactic acid and 3-indolepropionic acid levels were further confirmed using HPLC. This study provides a new perspective for the application of AOS as a feed additive against pathogenic intestinal bacteria. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s42995-023-00176-z. Springer Nature Singapore 2023-05-29 /pmc/articles/PMC10232696/ /pubmed/37275545 http://dx.doi.org/10.1007/s42995-023-00176-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Paper
Cheng, Jiaying
Xiao, Mengshi
Ren, Xinmiao
Secundo, Francesco
Yu, Ying
Nan, Shihao
Chen, Weimiao
Zhu, Changliang
Kong, Qing
Huang, Youtao
Fu, Xiaodan
Mou, Haijin
Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title_full Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title_fullStr Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title_full_unstemmed Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title_short Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
title_sort response of salmonella enterica serovar typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10232696/
https://www.ncbi.nlm.nih.gov/pubmed/37275545
http://dx.doi.org/10.1007/s42995-023-00176-z
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