Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls
Abstract Background Many countries have already banned the use of antibiotics in animal husbandry, making it extremely difficult to maintain animal health in livestock breeding. In the livestock industry, there is an urgent need to develop alternatives to antibiotics which will not lead to drug resi...
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| Format: | Article |
| Language: | English |
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BMC
2023-03-01
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| Series: | Journal of Animal Science and Biotechnology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40104-023-00832-5 |
| _version_ | 1797863975458701312 |
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| author | Jinping Shi Yu Lei Jianping Wu Zemin Li Xiao Zhang Li Jia Ying Wang Yue Ma Ke Zhang Qiang Cheng Zhao Zhang Yannan Ma Zhaomin Lei |
| author_facet | Jinping Shi Yu Lei Jianping Wu Zemin Li Xiao Zhang Li Jia Ying Wang Yue Ma Ke Zhang Qiang Cheng Zhao Zhang Yannan Ma Zhaomin Lei |
| author_sort | Jinping Shi |
| collection | DOAJ |
| description | Abstract Background Many countries have already banned the use of antibiotics in animal husbandry, making it extremely difficult to maintain animal health in livestock breeding. In the livestock industry, there is an urgent need to develop alternatives to antibiotics which will not lead to drug resistance on prolonged use. In this study, eighteen castrated bulls were randomly divided into two groups. The control group (CK) was fed the basal diet, while the antimicrobial peptide group (AP) was fed the basal diet supplemented with 8 g of antimicrobial peptides in the basal diet for the experimental period of 270 d. They were then slaughtered to measure production performance, and the ruminal contents were isolated for metagenomic and metabolome sequencing analysis. Result The results showed that antimicrobial peptides could improve the daily weight, carcass weight, and net meat weight of the experimental animals. Additionally, the rumen papillae diameter and the micropapillary density in the AP were significantly greater than those in the CK. Furthermore, the determination of digestive enzymes and fermentation parameters showed that the contents of protease, xylanase, and β-glucoside in the AP were greater than those in the CK. However, lipase content in the CK was greater than that in the AP. Moreover, the content of acetate, propionate, butyrate, and valerate was found to be greater in AP than those in CK. The metagenomic analysis annotated 1993 differential microorganisms at the species level. The KEGG enrichment of these microorganisms revealed that the enrichment of drug resistance-related pathways was dramatically decreased in the AP, whereas the enrichment of immune-related pathways was significantly increased. There was also a significant reduction in the types of viruses in the AP. 187 probiotics with significant differences were found, 135 of which were higher in AP than in CK. It was also found that the antimicrobial mechanism of the antimicrobial peptides was quite specific. Seven low-abundance microorganisms (Acinetobacter_sp._Ac_1271, Aequorivita soesokkakensis, Bacillus lacisalsi, Haloferax larsenii, Lysinibacillus_sp._3DF0063, Parabacteroides_sp._2_1_7, Streptomyces_sp._So13.3) were found to regulate growth performance of the bull negatively. Metabolome analysis identified 45 differentially differential metabolites that significantly different between the CK and the AP groups. Seven upregulated metabolites (4-pyridoxic acid, Ala-Phe, 3-ureidopropionate, hippuric acid, terephthalic acid, L-alanine, uridine 5-monophosphate) improve the growth performance of the experimental animals. To detect the interactions between the rumen microbiome and metabolism, we associated the rumen microbiome with the metabolome and found that negative regulation between the above 7 microorganisms and 7 metabolites. Conclusions This study shows that antimicrobial peptides can improve the growth performance of animals while resisting viruses and harmful bacteria and are expected to become healthy alternatives to antibiotics. We demonstrated a new antimicrobial peptides pharmacological model. We demonstrated low-abundance microorganisms may play a role by regulating the content of metabolites. |
| first_indexed | 2024-04-09T22:44:09Z |
| format | Article |
| id | doaj.art-c21cac0dbbc44893b9b336397df1e2ad |
| institution | Directory Open Access Journal |
| issn | 2049-1891 |
| language | English |
| last_indexed | 2024-04-09T22:44:09Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Animal Science and Biotechnology |
| spelling | doaj.art-c21cac0dbbc44893b9b336397df1e2ad2023-03-22T12:00:04ZengBMCJournal of Animal Science and Biotechnology2049-18912023-03-0114111710.1186/s40104-023-00832-5Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bullsJinping Shi0Yu Lei1Jianping Wu2Zemin Li3Xiao Zhang4Li Jia5Ying Wang6Yue Ma7Ke Zhang8Qiang Cheng9Zhao Zhang10Yannan Ma11Zhaomin Lei12College of Animal Science and Technology, Gansu Agricultural UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shanxi Province, College of Animal Science and Technology, Northwest A&F UniversityInstitute of Rural Development, Northwest Normal UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shanxi Province, College of Animal Science and Technology, Northwest A&F UniversityJingchuan Xu Kang Food Co.Gansu Huarui Agriculture Co.Institute of Rural Development, Northwest Normal UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityAbstract Background Many countries have already banned the use of antibiotics in animal husbandry, making it extremely difficult to maintain animal health in livestock breeding. In the livestock industry, there is an urgent need to develop alternatives to antibiotics which will not lead to drug resistance on prolonged use. In this study, eighteen castrated bulls were randomly divided into two groups. The control group (CK) was fed the basal diet, while the antimicrobial peptide group (AP) was fed the basal diet supplemented with 8 g of antimicrobial peptides in the basal diet for the experimental period of 270 d. They were then slaughtered to measure production performance, and the ruminal contents were isolated for metagenomic and metabolome sequencing analysis. Result The results showed that antimicrobial peptides could improve the daily weight, carcass weight, and net meat weight of the experimental animals. Additionally, the rumen papillae diameter and the micropapillary density in the AP were significantly greater than those in the CK. Furthermore, the determination of digestive enzymes and fermentation parameters showed that the contents of protease, xylanase, and β-glucoside in the AP were greater than those in the CK. However, lipase content in the CK was greater than that in the AP. Moreover, the content of acetate, propionate, butyrate, and valerate was found to be greater in AP than those in CK. The metagenomic analysis annotated 1993 differential microorganisms at the species level. The KEGG enrichment of these microorganisms revealed that the enrichment of drug resistance-related pathways was dramatically decreased in the AP, whereas the enrichment of immune-related pathways was significantly increased. There was also a significant reduction in the types of viruses in the AP. 187 probiotics with significant differences were found, 135 of which were higher in AP than in CK. It was also found that the antimicrobial mechanism of the antimicrobial peptides was quite specific. Seven low-abundance microorganisms (Acinetobacter_sp._Ac_1271, Aequorivita soesokkakensis, Bacillus lacisalsi, Haloferax larsenii, Lysinibacillus_sp._3DF0063, Parabacteroides_sp._2_1_7, Streptomyces_sp._So13.3) were found to regulate growth performance of the bull negatively. Metabolome analysis identified 45 differentially differential metabolites that significantly different between the CK and the AP groups. Seven upregulated metabolites (4-pyridoxic acid, Ala-Phe, 3-ureidopropionate, hippuric acid, terephthalic acid, L-alanine, uridine 5-monophosphate) improve the growth performance of the experimental animals. To detect the interactions between the rumen microbiome and metabolism, we associated the rumen microbiome with the metabolome and found that negative regulation between the above 7 microorganisms and 7 metabolites. Conclusions This study shows that antimicrobial peptides can improve the growth performance of animals while resisting viruses and harmful bacteria and are expected to become healthy alternatives to antibiotics. We demonstrated a new antimicrobial peptides pharmacological model. We demonstrated low-abundance microorganisms may play a role by regulating the content of metabolites.https://doi.org/10.1186/s40104-023-00832-5Antimicrobial peptidesCastrated bullGrowth performanceMetabolitesMicroorganismsRumen |
| spellingShingle | Jinping Shi Yu Lei Jianping Wu Zemin Li Xiao Zhang Li Jia Ying Wang Yue Ma Ke Zhang Qiang Cheng Zhao Zhang Yannan Ma Zhaomin Lei Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls Journal of Animal Science and Biotechnology Antimicrobial peptides Castrated bull Growth performance Metabolites Microorganisms Rumen |
| title | Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| title_full | Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| title_fullStr | Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| title_full_unstemmed | Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| title_short | Antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| title_sort | antimicrobial peptides act on the rumen microbiome and metabolome affecting the performance of castrated bulls |
| topic | Antimicrobial peptides Castrated bull Growth performance Metabolites Microorganisms Rumen |
| url | https://doi.org/10.1186/s40104-023-00832-5 |
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