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Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium

BACKGROUND: Salmonella Typhimurium challenge causes a huge detriment to chicken production. N-acyl homoserine lactonase (AHLase), a quorum quenching enzyme, potentially inhibits the growth and virulence of Gram-negative bacteria. However, it is unknown whether AHLase can protect chickens against S....

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Autores principales: Wang, Weiwei, Ou, Jingseng, Ye, Hui, Cao, Qingyun, Zhang, Changming, Dong, Zemin, Feng, Dingyuan, Zuo, Jianjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9827655/
https://www.ncbi.nlm.nih.gov/pubmed/36617579
http://dx.doi.org/10.1186/s40104-022-00801-4
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author Wang, Weiwei
Ou, Jingseng
Ye, Hui
Cao, Qingyun
Zhang, Changming
Dong, Zemin
Feng, Dingyuan
Zuo, Jianjun
author_facet Wang, Weiwei
Ou, Jingseng
Ye, Hui
Cao, Qingyun
Zhang, Changming
Dong, Zemin
Feng, Dingyuan
Zuo, Jianjun
author_sort Wang, Weiwei
collection PubMed
description BACKGROUND: Salmonella Typhimurium challenge causes a huge detriment to chicken production. N-acyl homoserine lactonase (AHLase), a quorum quenching enzyme, potentially inhibits the growth and virulence of Gram-negative bacteria. However, it is unknown whether AHLase can protect chickens against S. Typhimurium challenge. This study aimed to evaluate the effects of AHLase on growth performance and intestinal health in broilers challenged by S. Typhimurium. A total of 240 one-day-old female crossbred broilers (817C) were randomly divided into 5 groups (6 replicates/group): negative control (NC), positive control (PC), and PC group supplemented with 5, 10 or 20 U/g AHLase. All birds except those in NC were challenged with S. Typhimurium from 7 to 9 days of age. All parameters related to growth and intestinal health were determined on d 10 and 14. RESULTS: The reductions (P < 0.05) in body weight (BW) and average daily gain (ADG) in challenged birds were alleviated by AHLase addition especially at 10 U/g. Thus, samples from NC, PC and PC plus 10 U/g AHLase group were selected for further analysis. S. Typhimurium challenge impaired (P < 0.05) intestinal morphology, elevated (P < 0.05) ileal inflammatory cytokines (IL-1β and IL-8) expression, and increased (P < 0.05) serum diamine oxidase (DAO) activity on d 10. However, AHLase addition normalized these changes. Gut microbiota analysis on d 10 showed that AHLase reversed the reductions (P < 0.05) in several beneficial bacteria (e.g. Bacilli, Bacillales and Lactobacillales), along with increases (P < 0.05) in certain harmful bacteria (e.g. Proteobacteria, Gammaproteobacteria, Enterobacteriaceae and Escherichia/Shigella) in PC group. Furthermore, AHLase-induced increased beneficial bacteria and decreased harmful bacteria were basically negatively correlated (P < 0.05) with the reductions of ileal IL-1β and IL-8 expression and serum DAO activity, but positively correlated (P < 0.05) with the increased BW and ADG. Functional prediction revealed that AHLase abolished S. Typhimurium-induced upregulations (P < 0.05) of certain pathogenicity-related pathways such as lipopolysaccharide biosynthesis, shigellosis, bacterial invasion of epithelial cells and pathogenic Escherichia coli infection of gut microbiota. CONCLUSIONS: Supplemental AHLase attenuated S. Typhimurium-induced growth retardation and intestinal disruption in broilers, which could be associated with the observed recovery of gut microbiota dysbiosis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00801-4.
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spelling pubmed-98276552023-01-10 Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium Wang, Weiwei Ou, Jingseng Ye, Hui Cao, Qingyun Zhang, Changming Dong, Zemin Feng, Dingyuan Zuo, Jianjun J Anim Sci Biotechnol Research BACKGROUND: Salmonella Typhimurium challenge causes a huge detriment to chicken production. N-acyl homoserine lactonase (AHLase), a quorum quenching enzyme, potentially inhibits the growth and virulence of Gram-negative bacteria. However, it is unknown whether AHLase can protect chickens against S. Typhimurium challenge. This study aimed to evaluate the effects of AHLase on growth performance and intestinal health in broilers challenged by S. Typhimurium. A total of 240 one-day-old female crossbred broilers (817C) were randomly divided into 5 groups (6 replicates/group): negative control (NC), positive control (PC), and PC group supplemented with 5, 10 or 20 U/g AHLase. All birds except those in NC were challenged with S. Typhimurium from 7 to 9 days of age. All parameters related to growth and intestinal health were determined on d 10 and 14. RESULTS: The reductions (P < 0.05) in body weight (BW) and average daily gain (ADG) in challenged birds were alleviated by AHLase addition especially at 10 U/g. Thus, samples from NC, PC and PC plus 10 U/g AHLase group were selected for further analysis. S. Typhimurium challenge impaired (P < 0.05) intestinal morphology, elevated (P < 0.05) ileal inflammatory cytokines (IL-1β and IL-8) expression, and increased (P < 0.05) serum diamine oxidase (DAO) activity on d 10. However, AHLase addition normalized these changes. Gut microbiota analysis on d 10 showed that AHLase reversed the reductions (P < 0.05) in several beneficial bacteria (e.g. Bacilli, Bacillales and Lactobacillales), along with increases (P < 0.05) in certain harmful bacteria (e.g. Proteobacteria, Gammaproteobacteria, Enterobacteriaceae and Escherichia/Shigella) in PC group. Furthermore, AHLase-induced increased beneficial bacteria and decreased harmful bacteria were basically negatively correlated (P < 0.05) with the reductions of ileal IL-1β and IL-8 expression and serum DAO activity, but positively correlated (P < 0.05) with the increased BW and ADG. Functional prediction revealed that AHLase abolished S. Typhimurium-induced upregulations (P < 0.05) of certain pathogenicity-related pathways such as lipopolysaccharide biosynthesis, shigellosis, bacterial invasion of epithelial cells and pathogenic Escherichia coli infection of gut microbiota. CONCLUSIONS: Supplemental AHLase attenuated S. Typhimurium-induced growth retardation and intestinal disruption in broilers, which could be associated with the observed recovery of gut microbiota dysbiosis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00801-4. BioMed Central 2023-01-09 /pmc/articles/PMC9827655/ /pubmed/36617579 http://dx.doi.org/10.1186/s40104-022-00801-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wang, Weiwei
Ou, Jingseng
Ye, Hui
Cao, Qingyun
Zhang, Changming
Dong, Zemin
Feng, Dingyuan
Zuo, Jianjun
Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title_full Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title_fullStr Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title_full_unstemmed Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title_short Supplemental N-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by Salmonella Typhimurium
title_sort supplemental n-acyl homoserine lactonase alleviates intestinal disruption and improves gut microbiota in broilers challenged by salmonella typhimurium
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9827655/
https://www.ncbi.nlm.nih.gov/pubmed/36617579
http://dx.doi.org/10.1186/s40104-022-00801-4
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