Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens
Abstract Background Salpingitis is one of the common diseases in laying hen production, which greatly decreases the economic outcome of laying hen farming. Lactiplantibacillus plantarum was effective in preventing local or systemic inflammation, however rare studies were reported on its prevention a...
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | Journal of Animal Science and Biotechnology |
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| Online Access: | https://doi.org/10.1186/s40104-023-00937-x |
| _version_ | 1827709182938185728 |
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| author | Dan Song Aike Li Bingxu Chen Jia Feng Tao Duan Junlin Cheng Lixian Chen Weiwei Wang Yuna Min |
| author_facet | Dan Song Aike Li Bingxu Chen Jia Feng Tao Duan Junlin Cheng Lixian Chen Weiwei Wang Yuna Min |
| author_sort | Dan Song |
| collection | DOAJ |
| description | Abstract Background Salpingitis is one of the common diseases in laying hen production, which greatly decreases the economic outcome of laying hen farming. Lactiplantibacillus plantarum was effective in preventing local or systemic inflammation, however rare studies were reported on its prevention against salpingitis. This study aimed to investigate the preventive molecular regulatory network of microencapsulated Lactiplantibacillus plantarum (MLP) against salpingitis through multi-omics analysis, including microbiome, transcriptome and metabolome analyses. Results The results revealed that supplementation of MLP in diet significantly alleviated the inflammation and atrophy of uterus caused by lipopolysaccharide (LPS) in hens (P < 0.05). The concentrations of plasma IL-2 and IL-10 in hens of MLP-LPS group were higher than those in hens of LPS-stimulation group (CN-LPS group) (P < 0.05). The expression levels of TLR2, MYD88, NF-κB, COX2, and TNF-α were significantly decreased in the hens fed diet supplemented with MLP and suffered with LPS stimulation (MLP-LPS group) compared with those in the hens of CN-LPS group (P < 0.05). Differentially expressed genes (DEGs) induced by MLP were involved in inflammation, reproduction, and calcium ion transport. At the genus level, the MLP supplementation significantly increased the abundance of Phascolarctobacterium, whereas decreased the abundance of Candidatus_Saccharimonas in LPS challenged hens (P < 0.05). The metabolites altered by dietary supplementation with MLP were mainly involved in galactose, uronic acid, histidine, pyruvate and primary bile acid metabolism. Dietary supplementation with MLP inversely regulates LPS-induced differential metabolites such as LysoPA (24:0/0:0) (P < 0.05). Conclusions In summary, dietary supplementation with microencapsulated Lactiplantibacillus plantarum prevented salpingitis by modulating the abundances of Candidatus_Saccharimonas, Phascolarctobacterium, Ruminococcus_torques_group and Eubacterium_hallii_group while downregulating the levels of plasma metabolites, p-tolyl sulfate, o-cresol and N-acetylhistamine and upregulating S-lactoylglutathione, simultaneously increasing the expressions of CPNE4, CNTN3 and ACAN genes in the uterus, and ultimately inhibiting oviducal inflammation. |
| first_indexed | 2024-03-10T17:17:21Z |
| format | Article |
| id | doaj.art-961b005e997b4d35aa91006ff6e0be98 |
| institution | Directory Open Access Journal |
| issn | 2049-1891 |
| language | English |
| last_indexed | 2024-03-10T17:17:21Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
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| series | Journal of Animal Science and Biotechnology |
| spelling | doaj.art-961b005e997b4d35aa91006ff6e0be982023-11-20T10:28:34ZengBMCJournal of Animal Science and Biotechnology2049-18912023-11-0114111510.1186/s40104-023-00937-xMulti-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hensDan Song0Aike Li1Bingxu Chen2Jia Feng3Tao Duan4Junlin Cheng5Lixian Chen6Weiwei Wang7Yuna Min8College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Grain and Oil Biotechnology of National Food and Strategic Reserves Administration, Academy of National Food and Strategic Reserves AdministrationCollege of Animal Science and Technology, Northwest A&F UniversityCollege of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Grain and Oil Biotechnology of National Food and Strategic Reserves Administration, Academy of National Food and Strategic Reserves AdministrationKey Laboratory of Grain and Oil Biotechnology of National Food and Strategic Reserves Administration, Academy of National Food and Strategic Reserves AdministrationKey Laboratory of Grain and Oil Biotechnology of National Food and Strategic Reserves Administration, Academy of National Food and Strategic Reserves AdministrationKey Laboratory of Grain and Oil Biotechnology of National Food and Strategic Reserves Administration, Academy of National Food and Strategic Reserves AdministrationCollege of Animal Science and Technology, Northwest A&F UniversityAbstract Background Salpingitis is one of the common diseases in laying hen production, which greatly decreases the economic outcome of laying hen farming. Lactiplantibacillus plantarum was effective in preventing local or systemic inflammation, however rare studies were reported on its prevention against salpingitis. This study aimed to investigate the preventive molecular regulatory network of microencapsulated Lactiplantibacillus plantarum (MLP) against salpingitis through multi-omics analysis, including microbiome, transcriptome and metabolome analyses. Results The results revealed that supplementation of MLP in diet significantly alleviated the inflammation and atrophy of uterus caused by lipopolysaccharide (LPS) in hens (P < 0.05). The concentrations of plasma IL-2 and IL-10 in hens of MLP-LPS group were higher than those in hens of LPS-stimulation group (CN-LPS group) (P < 0.05). The expression levels of TLR2, MYD88, NF-κB, COX2, and TNF-α were significantly decreased in the hens fed diet supplemented with MLP and suffered with LPS stimulation (MLP-LPS group) compared with those in the hens of CN-LPS group (P < 0.05). Differentially expressed genes (DEGs) induced by MLP were involved in inflammation, reproduction, and calcium ion transport. At the genus level, the MLP supplementation significantly increased the abundance of Phascolarctobacterium, whereas decreased the abundance of Candidatus_Saccharimonas in LPS challenged hens (P < 0.05). The metabolites altered by dietary supplementation with MLP were mainly involved in galactose, uronic acid, histidine, pyruvate and primary bile acid metabolism. Dietary supplementation with MLP inversely regulates LPS-induced differential metabolites such as LysoPA (24:0/0:0) (P < 0.05). Conclusions In summary, dietary supplementation with microencapsulated Lactiplantibacillus plantarum prevented salpingitis by modulating the abundances of Candidatus_Saccharimonas, Phascolarctobacterium, Ruminococcus_torques_group and Eubacterium_hallii_group while downregulating the levels of plasma metabolites, p-tolyl sulfate, o-cresol and N-acetylhistamine and upregulating S-lactoylglutathione, simultaneously increasing the expressions of CPNE4, CNTN3 and ACAN genes in the uterus, and ultimately inhibiting oviducal inflammation.https://doi.org/10.1186/s40104-023-00937-xLaying henMetabolomeMicrobiomeMicroencapsulated Lactiplantibacillus plantarumSalpingitisTranscriptome |
| spellingShingle | Dan Song Aike Li Bingxu Chen Jia Feng Tao Duan Junlin Cheng Lixian Chen Weiwei Wang Yuna Min Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens Journal of Animal Science and Biotechnology Laying hen Metabolome Microbiome Microencapsulated Lactiplantibacillus plantarum Salpingitis Transcriptome |
| title | Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens |
| title_full | Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens |
| title_fullStr | Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens |
| title_full_unstemmed | Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens |
| title_short | Multi-omics analysis reveals the molecular regulatory network underlying the prevention of Lactiplantibacillus plantarum against LPS-induced salpingitis in laying hens |
| title_sort | multi omics analysis reveals the molecular regulatory network underlying the prevention of lactiplantibacillus plantarum against lps induced salpingitis in laying hens |
| topic | Laying hen Metabolome Microbiome Microencapsulated Lactiplantibacillus plantarum Salpingitis Transcriptome |
| url | https://doi.org/10.1186/s40104-023-00937-x |
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