Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits

Abstract Background Antimicrobial resistance is one of the most urgent threat to global public health, as it can lead to high morbidity, mortality, and medical costs for humans and livestock animals. In ruminants, the rumen microbiome carries a large number of antimicrobial resistance genes (ARGs),...

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Main Authors: Ming-Yuan Xue, Yun-Yi Xie, Yi-Fan Zhong, Jian-Xin Liu, Le Luo Guan, Hui-Zeng Sun
Format: Article
Language:English
Published: BMC 2021-02-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-021-00081-9
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author Ming-Yuan Xue
Yun-Yi Xie
Yi-Fan Zhong
Jian-Xin Liu
Le Luo Guan
Hui-Zeng Sun
author_facet Ming-Yuan Xue
Yun-Yi Xie
Yi-Fan Zhong
Jian-Xin Liu
Le Luo Guan
Hui-Zeng Sun
author_sort Ming-Yuan Xue
collection DOAJ
description Abstract Background Antimicrobial resistance is one of the most urgent threat to global public health, as it can lead to high morbidity, mortality, and medical costs for humans and livestock animals. In ruminants, the rumen microbiome carries a large number of antimicrobial resistance genes (ARGs), which could disseminate to the environment through saliva, or through the flow of rumen microbial biomass to the hindgut and released through feces. The occurrence and distribution of ARGs in rumen microbes has been reported, revealing the effects of external stimuli (e.g., antimicrobial administrations and diet ingredients) on the antimicrobial resistance in the rumen. However, the host effect on the ruminal resistome and their interactions remain largely unknown. Here, we investigated the ruminal resistome and its relationship with host feed intake and milk protein yield using metagenomic sequencing. Results The ruminal resistome conferred resistance to 26 classes of antimicrobials, with genes encoding resistance to tetracycline being the most predominant. The ARG-containing contigs were assigned to bacterial taxonomy, and the majority of highly abundant bacterial genera were resistant to at least one antimicrobial, while the abundances of ARG-containing bacterial genera showed distinct variations. Although the ruminal resistome is not co-varied with host feed intake, it could be potentially linked to milk protein yield in dairy cows. Results showed that host feed intake did not affect the alpha or beta diversity of the ruminal resistome or the abundances of ARGs, while the Shannon index (R 2  = 0.63, P < 0.01) and richness (R 2  = 0.67, P < 0.01) of the ruminal resistome were highly correlated with milk protein yield. A total of 128 significantly different ARGs (FDR < 0.05) were identified in the high- and low-milk protein yield dairy cows. We found four ruminal resistotypes that are driven by specific ARGs and associated with milk protein yield. Particularly, cows with low milk protein yield are classified into the same ruminal resistotype and featured by high-abundance ARGs, including mfd and sav1866. Conclusions The current study uncovered the prevalence of ARGs in the rumen of a cohort of lactating dairy cows. The ruminal resistome is not co-varied with host feed intake, while it could be potentially linked to milk protein yield in dairy cows. Our results provide fundamental knowledge on the prevalence, mechanisms and impact factors of antimicrobial resistance in dairy cattle and are important for both the dairy industry and other food animal antimicrobial resistance control strategies.
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spelling doaj.art-04847e130b4b4b35b6629debab6aaf192022-12-21T23:01:46ZengBMCAnimal Microbiome2524-46712021-02-013111710.1186/s42523-021-00081-9Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traitsMing-Yuan Xue0Yun-Yi Xie1Yi-Fan Zhong2Jian-Xin Liu3Le Luo Guan4Hui-Zeng Sun5Institute of Dairy Science, Ministry of Education Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang UniversityInstitute of Dairy Science, Ministry of Education Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang UniversityInstitute of Dairy Science, Ministry of Education Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang UniversityInstitute of Dairy Science, Ministry of Education Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang UniversityDepartment of Agricultural, Food and Nutritional Science, University of AlbertaInstitute of Dairy Science, Ministry of Education Key Laboratory of Molecular Animal Nutrition, College of Animal Sciences, Zhejiang UniversityAbstract Background Antimicrobial resistance is one of the most urgent threat to global public health, as it can lead to high morbidity, mortality, and medical costs for humans and livestock animals. In ruminants, the rumen microbiome carries a large number of antimicrobial resistance genes (ARGs), which could disseminate to the environment through saliva, or through the flow of rumen microbial biomass to the hindgut and released through feces. The occurrence and distribution of ARGs in rumen microbes has been reported, revealing the effects of external stimuli (e.g., antimicrobial administrations and diet ingredients) on the antimicrobial resistance in the rumen. However, the host effect on the ruminal resistome and their interactions remain largely unknown. Here, we investigated the ruminal resistome and its relationship with host feed intake and milk protein yield using metagenomic sequencing. Results The ruminal resistome conferred resistance to 26 classes of antimicrobials, with genes encoding resistance to tetracycline being the most predominant. The ARG-containing contigs were assigned to bacterial taxonomy, and the majority of highly abundant bacterial genera were resistant to at least one antimicrobial, while the abundances of ARG-containing bacterial genera showed distinct variations. Although the ruminal resistome is not co-varied with host feed intake, it could be potentially linked to milk protein yield in dairy cows. Results showed that host feed intake did not affect the alpha or beta diversity of the ruminal resistome or the abundances of ARGs, while the Shannon index (R 2  = 0.63, P < 0.01) and richness (R 2  = 0.67, P < 0.01) of the ruminal resistome were highly correlated with milk protein yield. A total of 128 significantly different ARGs (FDR < 0.05) were identified in the high- and low-milk protein yield dairy cows. We found four ruminal resistotypes that are driven by specific ARGs and associated with milk protein yield. Particularly, cows with low milk protein yield are classified into the same ruminal resistotype and featured by high-abundance ARGs, including mfd and sav1866. Conclusions The current study uncovered the prevalence of ARGs in the rumen of a cohort of lactating dairy cows. The ruminal resistome is not co-varied with host feed intake, while it could be potentially linked to milk protein yield in dairy cows. Our results provide fundamental knowledge on the prevalence, mechanisms and impact factors of antimicrobial resistance in dairy cattle and are important for both the dairy industry and other food animal antimicrobial resistance control strategies.https://doi.org/10.1186/s42523-021-00081-9Dairy cattleRumenMetagenomicsResistomeMicrobiome
spellingShingle Ming-Yuan Xue
Yun-Yi Xie
Yi-Fan Zhong
Jian-Xin Liu
Le Luo Guan
Hui-Zeng Sun
Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
Animal Microbiome
Dairy cattle
Rumen
Metagenomics
Resistome
Microbiome
title Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
title_full Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
title_fullStr Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
title_full_unstemmed Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
title_short Ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
title_sort ruminal resistome of dairy cattle is individualized and the resistotypes are associated with milking traits
topic Dairy cattle
Rumen
Metagenomics
Resistome
Microbiome
url https://doi.org/10.1186/s42523-021-00081-9
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