Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids
Abstract Background The gut microbiome of domestic animals carries antibiotic resistance genes (ARGs) which can be transmitted to the environment and humans, resulting in challenges of antibiotic resistance. Although it has been reported that the rumen microbiome of ruminants may be a reservoir of A...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01733-5 |
| _version_ | 1797276395643076608 |
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| author | Jianmin Chai Yimin Zhuang Kai Cui Yanliang Bi Naifeng Zhang |
| author_facet | Jianmin Chai Yimin Zhuang Kai Cui Yanliang Bi Naifeng Zhang |
| author_sort | Jianmin Chai |
| collection | DOAJ |
| description | Abstract Background The gut microbiome of domestic animals carries antibiotic resistance genes (ARGs) which can be transmitted to the environment and humans, resulting in challenges of antibiotic resistance. Although it has been reported that the rumen microbiome of ruminants may be a reservoir of ARGs, the factors affecting the temporal dynamics of the rumen resistome are still unclear. Here, we collected rumen content samples of goats at 1, 7, 14, 28, 42, 56, 70, and 84 days of age, analyzed their microbiome and resistome profiles using metagenomics, and assessed the temporal dynamics of the rumen resistome in goats at the early stage of life under a conventional feeding system. Results In our results, the rumen resistome of goat kids contained ARGs to 41 classes, and the richness of ARGs decreased with age. Four antibiotic compound types of ARGs, including drugs, biocides, metals, and multi-compounds, were found during milk feeding, while only drug types of ARGs were observed after supplementation with starter feed. The specific ARGs for each age and their temporal dynamics were characterized, and the network inference model revealed that the interactions among ARGs were related to age. A strong correlation between the profiles of rumen resistome and microbiome was found using Procrustes analysis. Ruminal Escherichia coli within Proteobacteria phylum was the main carrier of ARGs in goats consuming colostrum, while Prevotella ruminicola and Fibrobacter succinogenes associated with cellulose degradation were the carriers of ARGs after starter supplementation. Milk consumption was likely a source of rumen ARGs, and the changes in the rumen resistome with age were correlated with the microbiome modulation by starter supplementation. Conclusions Our data revealed that the temporal dynamics of the rumen resistome are associated with the microbiome, and the reservoir of ARGs in the rumen during early life is likely related to age and diet. It may be a feasible strategy to reduce the rumen and its downstream dissemination of ARGs in ruminants through early-life dietary intervention. Video Abstract |
| first_indexed | 2024-03-07T15:27:41Z |
| format | Article |
| id | doaj.art-5662e4ad249540f79fff719c789c39d0 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-07T15:27:41Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-5662e4ad249540f79fff719c789c39d02024-03-05T16:36:15ZengBMCMicrobiome2049-26182024-01-0112111810.1186/s40168-023-01733-5Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kidsJianmin Chai0Yimin Zhuang1Kai Cui2Yanliang Bi3Naifeng Zhang4Institute of Feed Research of Chinese Academy of Agricultural Sciences, Key Laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural AffairsInstitute of Feed Research of Chinese Academy of Agricultural Sciences, Key Laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural AffairsInstitute of Feed Research of Chinese Academy of Agricultural Sciences, Key Laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural AffairsInstitute of Feed Research of Chinese Academy of Agricultural Sciences, Key Laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural AffairsInstitute of Feed Research of Chinese Academy of Agricultural Sciences, Key Laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural AffairsAbstract Background The gut microbiome of domestic animals carries antibiotic resistance genes (ARGs) which can be transmitted to the environment and humans, resulting in challenges of antibiotic resistance. Although it has been reported that the rumen microbiome of ruminants may be a reservoir of ARGs, the factors affecting the temporal dynamics of the rumen resistome are still unclear. Here, we collected rumen content samples of goats at 1, 7, 14, 28, 42, 56, 70, and 84 days of age, analyzed their microbiome and resistome profiles using metagenomics, and assessed the temporal dynamics of the rumen resistome in goats at the early stage of life under a conventional feeding system. Results In our results, the rumen resistome of goat kids contained ARGs to 41 classes, and the richness of ARGs decreased with age. Four antibiotic compound types of ARGs, including drugs, biocides, metals, and multi-compounds, were found during milk feeding, while only drug types of ARGs were observed after supplementation with starter feed. The specific ARGs for each age and their temporal dynamics were characterized, and the network inference model revealed that the interactions among ARGs were related to age. A strong correlation between the profiles of rumen resistome and microbiome was found using Procrustes analysis. Ruminal Escherichia coli within Proteobacteria phylum was the main carrier of ARGs in goats consuming colostrum, while Prevotella ruminicola and Fibrobacter succinogenes associated with cellulose degradation were the carriers of ARGs after starter supplementation. Milk consumption was likely a source of rumen ARGs, and the changes in the rumen resistome with age were correlated with the microbiome modulation by starter supplementation. Conclusions Our data revealed that the temporal dynamics of the rumen resistome are associated with the microbiome, and the reservoir of ARGs in the rumen during early life is likely related to age and diet. It may be a feasible strategy to reduce the rumen and its downstream dissemination of ARGs in ruminants through early-life dietary intervention. Video Abstracthttps://doi.org/10.1186/s40168-023-01733-5Rumen resistomeMetagenomicsMicrobiomeRuminantsAgesTemporal dynamics |
| spellingShingle | Jianmin Chai Yimin Zhuang Kai Cui Yanliang Bi Naifeng Zhang Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids Microbiome Rumen resistome Metagenomics Microbiome Ruminants Ages Temporal dynamics |
| title | Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| title_full | Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| title_fullStr | Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| title_full_unstemmed | Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| title_short | Metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| title_sort | metagenomics reveals the temporal dynamics of the rumen resistome and microbiome in goat kids |
| topic | Rumen resistome Metagenomics Microbiome Ruminants Ages Temporal dynamics |
| url | https://doi.org/10.1186/s40168-023-01733-5 |
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