Feeding systems influence the rumen resistome in yaks by changing the microbiome

The rumen microbiome serves as a reservoir of antibiotic-resistance genes (ARGs) with significant implications for public health. This study aimed to investigate the effects of different feeding systems on the rumen resistome in yaks. Yaks that grazed naturally on pasture were used as controls, whil...

Full description

Saved in:
Bibliographic Details
Main Authors: Shuli Yang, Jialuo Chen, Jieyi Zheng, Huaming Mao, Feilong Deng, Dongwang Wu, Jianmin Chai
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1505938/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849344687132901376
author Shuli Yang
Jialuo Chen
Jieyi Zheng
Huaming Mao
Feilong Deng
Dongwang Wu
Jianmin Chai
author_facet Shuli Yang
Jialuo Chen
Jieyi Zheng
Huaming Mao
Feilong Deng
Dongwang Wu
Jianmin Chai
author_sort Shuli Yang
collection DOAJ
description The rumen microbiome serves as a reservoir of antibiotic-resistance genes (ARGs) with significant implications for public health. This study aimed to investigate the effects of different feeding systems on the rumen resistome in yaks. Yaks that grazed naturally on pasture were used as controls, while the experimental yaks were housed in a high-density pen environment and fed a specially designed diet to optimally meet their nutritional requirements, with increased interactions with farm workers. Metagenomic analysis was performed to assess changes in the rumen microbiome and resistome. Dietary factors influencing changes in the rumen microbiome and resistome were identified. A greater variety of microbiomes associated with carbohydrate digestion was found in yaks under a house-feeding system, such as Stomatobaculum longum and Succiniclasticum ruminis. Although grazing yaks exhibited various dominant antibiotic resistance genes (ARGs) at the class level, house-fed yaks were mainly enriched with tetracycline-resistant genes. A random forest model identified specific ARG signatures for each group, such as Sent_cmlA and Sliv_cmlR (Phenicol) and vanHD (Glycopeptide) prevalent in grazing yaks, while tet44, tetW, tetW/N/W, and tet40 were abundant in house-fed yaks. ARG interactions varied by feeding system, with signature ARGs in each group showing distinct correlations. Nevertheless, strong correlations among ARGs existed regardless of the treatments, such as the positive correlation between tetW and tetW/N/W in both groups. The rumen microbiome was strongly associated with the resistome, especially regarding abundant microbiomes and ARGs. Proteobacteria carrying ARGs were observed in grazing yaks, while Firmicutes served as hosts for ARGs in yaks under a housed feeding system. The specific bacteria contributing to the distinct ARGs in each group were identified. For instance, members of Firmicutes (Clostridium tepidiprofundi) carried their ARG signatures, such as tet44. These findings emphasized that diet, along with environmental factors and farmworker interactions, contributed to changes in the rumen resistome of yaks. This study is the first to discuss how multiple factors within a feeding regime influence the gut resistome, highlighting the drawbacks of intensive feedings with respect to the gut resistome.
format Article
id doaj-art-c2e0633a12804f1b84cd618e40a73bec
institution Kabale University
issn 1664-302X
language English
publishDate 2025-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj-art-c2e0633a12804f1b84cd618e40a73bec2025-08-20T03:42:37ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-03-011610.3389/fmicb.2025.15059381505938Feeding systems influence the rumen resistome in yaks by changing the microbiomeShuli Yang0Jialuo Chen1Jieyi Zheng2Huaming Mao3Feilong Deng4Dongwang Wu5Jianmin Chai6Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan, ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan, ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan, ChinaKey Laboratory of Animal Nutrition and Feed Science of Yunnan Province, Yunnan Agricultural University, Kunming, ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan, ChinaKey Laboratory of Animal Nutrition and Feed Science of Yunnan Province, Yunnan Agricultural University, Kunming, ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan, ChinaThe rumen microbiome serves as a reservoir of antibiotic-resistance genes (ARGs) with significant implications for public health. This study aimed to investigate the effects of different feeding systems on the rumen resistome in yaks. Yaks that grazed naturally on pasture were used as controls, while the experimental yaks were housed in a high-density pen environment and fed a specially designed diet to optimally meet their nutritional requirements, with increased interactions with farm workers. Metagenomic analysis was performed to assess changes in the rumen microbiome and resistome. Dietary factors influencing changes in the rumen microbiome and resistome were identified. A greater variety of microbiomes associated with carbohydrate digestion was found in yaks under a house-feeding system, such as Stomatobaculum longum and Succiniclasticum ruminis. Although grazing yaks exhibited various dominant antibiotic resistance genes (ARGs) at the class level, house-fed yaks were mainly enriched with tetracycline-resistant genes. A random forest model identified specific ARG signatures for each group, such as Sent_cmlA and Sliv_cmlR (Phenicol) and vanHD (Glycopeptide) prevalent in grazing yaks, while tet44, tetW, tetW/N/W, and tet40 were abundant in house-fed yaks. ARG interactions varied by feeding system, with signature ARGs in each group showing distinct correlations. Nevertheless, strong correlations among ARGs existed regardless of the treatments, such as the positive correlation between tetW and tetW/N/W in both groups. The rumen microbiome was strongly associated with the resistome, especially regarding abundant microbiomes and ARGs. Proteobacteria carrying ARGs were observed in grazing yaks, while Firmicutes served as hosts for ARGs in yaks under a housed feeding system. The specific bacteria contributing to the distinct ARGs in each group were identified. For instance, members of Firmicutes (Clostridium tepidiprofundi) carried their ARG signatures, such as tet44. These findings emphasized that diet, along with environmental factors and farmworker interactions, contributed to changes in the rumen resistome of yaks. This study is the first to discuss how multiple factors within a feeding regime influence the gut resistome, highlighting the drawbacks of intensive feedings with respect to the gut resistome.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1505938/fullantibioticsrumenmetagenomicsmicrobiomeruminantsresistome
spellingShingle Shuli Yang
Jialuo Chen
Jieyi Zheng
Huaming Mao
Feilong Deng
Dongwang Wu
Jianmin Chai
Feeding systems influence the rumen resistome in yaks by changing the microbiome
Frontiers in Microbiology
antibiotics
rumen
metagenomics
microbiome
ruminants
resistome
title Feeding systems influence the rumen resistome in yaks by changing the microbiome
title_full Feeding systems influence the rumen resistome in yaks by changing the microbiome
title_fullStr Feeding systems influence the rumen resistome in yaks by changing the microbiome
title_full_unstemmed Feeding systems influence the rumen resistome in yaks by changing the microbiome
title_short Feeding systems influence the rumen resistome in yaks by changing the microbiome
title_sort feeding systems influence the rumen resistome in yaks by changing the microbiome
topic antibiotics
rumen
metagenomics
microbiome
ruminants
resistome
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1505938/full
work_keys_str_mv AT shuliyang feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT jialuochen feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT jieyizheng feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT huamingmao feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT feilongdeng feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT dongwangwu feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome
AT jianminchai feedingsystemsinfluencetherumenresistomeinyaksbychangingthemicrobiome