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Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets

BACKGROUND: Lactic acid bacteria (LAB) participating in milk fermentation naturally release and enrich the fermented dairy product with a broad range of bioactive metabolites, which has numerous roles in the intestinal health-promoting of the consumer. However, information is lacking regarding the a...

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Autores principales: Lin, Ailian, Yan, Xiaoxi, Wang, Hongyu, Su, Yong, Zhu, Weiyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9536082/
https://www.ncbi.nlm.nih.gov/pubmed/36199127
http://dx.doi.org/10.1186/s40104-022-00762-8
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author Lin, Ailian
Yan, Xiaoxi
Wang, Hongyu
Su, Yong
Zhu, Weiyun
author_facet Lin, Ailian
Yan, Xiaoxi
Wang, Hongyu
Su, Yong
Zhu, Weiyun
author_sort Lin, Ailian
collection PubMed
description BACKGROUND: Lactic acid bacteria (LAB) participating in milk fermentation naturally release and enrich the fermented dairy product with a broad range of bioactive metabolites, which has numerous roles in the intestinal health-promoting of the consumer. However, information is lacking regarding the application prospect of LAB fermented milk in the animal industry. This study investigated the effects of lactic acid bacteria-fermented formula milk (LFM) on the growth performance, intestinal immunity, microbiota composition, and transcriptomic responses in weaned piglets. A total of 24 male weaned piglets were randomly divided into the control (CON) and LFM groups. Each group consisted of 6 replicates (cages) with 2 piglets per cage. Each piglet in the LFM group were supplemented with 80 mL LFM three times a day, while the CON group was treated with the same amount of drinking water. RESULTS: LFM significantly increased the average daily gain of piglets over the entire 14 d (P < 0.01) and the average daily feed intake from 7 to 14 d (P < 0.05). Compared to the CON group, ileal goblet cell count, villus-crypt ratio, sIgA, and lactate concentrations in the LFM group were significantly increased (P < 0.05). Transcriptomic analysis of ileal mucosa identified 487 differentially expressed genes (DEGs) between two groups. Especially, DEGs involved in the intestinal immune network for IgA production pathways, such as polymeric immunoglobulin receptor (PIGR), were significantly up-regulated (P < 0.01) by LFM supplementation. Moreover, trefoil factor 2 (TFF2) in the LFM group, one of the DEGs involved in the secretory function of goblet cells, was also significantly up-regulated (P < 0.01). Sequencing of the 16S rRNA gene of microbiota demonstrated that LFM led to selective enrichment of lactate-producing and short-chain fatty acid (SCFA)-producing bacteria in the ileum, such as an increase in the relative abundance of Enterococcus (P = 0.09) and Acetitomaculum (P < 0.05). CONCLUSIONS: LFM can improve intestinal health and immune tolerance, thus enhancing the growth performance of weaned piglets. The changes in microbiota and metabolites induced by LFM might mediate the regulation of the secretory function of goblet cells. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00762-8.
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spelling pubmed-95360822022-10-07 Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets Lin, Ailian Yan, Xiaoxi Wang, Hongyu Su, Yong Zhu, Weiyun J Anim Sci Biotechnol Research BACKGROUND: Lactic acid bacteria (LAB) participating in milk fermentation naturally release and enrich the fermented dairy product with a broad range of bioactive metabolites, which has numerous roles in the intestinal health-promoting of the consumer. However, information is lacking regarding the application prospect of LAB fermented milk in the animal industry. This study investigated the effects of lactic acid bacteria-fermented formula milk (LFM) on the growth performance, intestinal immunity, microbiota composition, and transcriptomic responses in weaned piglets. A total of 24 male weaned piglets were randomly divided into the control (CON) and LFM groups. Each group consisted of 6 replicates (cages) with 2 piglets per cage. Each piglet in the LFM group were supplemented with 80 mL LFM three times a day, while the CON group was treated with the same amount of drinking water. RESULTS: LFM significantly increased the average daily gain of piglets over the entire 14 d (P < 0.01) and the average daily feed intake from 7 to 14 d (P < 0.05). Compared to the CON group, ileal goblet cell count, villus-crypt ratio, sIgA, and lactate concentrations in the LFM group were significantly increased (P < 0.05). Transcriptomic analysis of ileal mucosa identified 487 differentially expressed genes (DEGs) between two groups. Especially, DEGs involved in the intestinal immune network for IgA production pathways, such as polymeric immunoglobulin receptor (PIGR), were significantly up-regulated (P < 0.01) by LFM supplementation. Moreover, trefoil factor 2 (TFF2) in the LFM group, one of the DEGs involved in the secretory function of goblet cells, was also significantly up-regulated (P < 0.01). Sequencing of the 16S rRNA gene of microbiota demonstrated that LFM led to selective enrichment of lactate-producing and short-chain fatty acid (SCFA)-producing bacteria in the ileum, such as an increase in the relative abundance of Enterococcus (P = 0.09) and Acetitomaculum (P < 0.05). CONCLUSIONS: LFM can improve intestinal health and immune tolerance, thus enhancing the growth performance of weaned piglets. The changes in microbiota and metabolites induced by LFM might mediate the regulation of the secretory function of goblet cells. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00762-8. BioMed Central 2022-10-06 /pmc/articles/PMC9536082/ /pubmed/36199127 http://dx.doi.org/10.1186/s40104-022-00762-8 Text en © The Author(s) 2022 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
Lin, Ailian
Yan, Xiaoxi
Wang, Hongyu
Su, Yong
Zhu, Weiyun
Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title_full Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title_fullStr Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title_full_unstemmed Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title_short Effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
title_sort effects of lactic acid bacteria-fermented formula milk supplementation on ileal microbiota, transcriptomic profile, and mucosal immunity in weaned piglets
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9536082/
https://www.ncbi.nlm.nih.gov/pubmed/36199127
http://dx.doi.org/10.1186/s40104-022-00762-8
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