A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.

Mounting evidence suggests that the gut microbiota plays an important role in the pathogenesis of mastitis, an important disease affecting the health of lactating women and the development of the dairy industry. However, the effect of the regulation of the gut microbiota by dietary components on mas...

Full description

Bibliographic Details
Main Authors: Caijun Zhao, Lijuan Bao, Yihong Zhao, Keyi Wu, Min Qiu, Lianjun Feng, Naisheng Zhang, Xiaoyu Hu, Yunhe Fu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1011108
_version_ 1797904215194992640
author Caijun Zhao
Lijuan Bao
Yihong Zhao
Keyi Wu
Min Qiu
Lianjun Feng
Naisheng Zhang
Xiaoyu Hu
Yunhe Fu
author_facet Caijun Zhao
Lijuan Bao
Yihong Zhao
Keyi Wu
Min Qiu
Lianjun Feng
Naisheng Zhang
Xiaoyu Hu
Yunhe Fu
author_sort Caijun Zhao
collection DOAJ
description Mounting evidence suggests that the gut microbiota plays an important role in the pathogenesis of mastitis, an important disease affecting the health of lactating women and the development of the dairy industry. However, the effect of the regulation of the gut microbiota by dietary components on mastitis development remains unknown. In this study, we found that a fiber-enriched diet alleviated Staphylococcus aureus (S. au)-induced mastitis in mice, which was dependent on the gut microbiota as depletion of the gut microbiota by antibiotics abolished this protective effect. Likewise, fecal microbiota transplantation (FMT) from high-inulin (HI)-treated mice (HIF) to recipient mice improved S. au-induced mastitis in mice. Consumption of an HI diet and HIF increased fecal short-chain fatty acid (SCFA) levels compared with the control group. Moreover, treatment with SCFAs, especially butyrate, alleviated S. au-induced mastitis in mice. Mechanistically, consumption of an HI diet enhanced the host antimicrobial program in macrophages through inhibiting histone deacetylase 3 by the production of butyrate. Collectively, our results suggest that modulation of the gut microbiota and its metabolism by dietary components is a potential strategy for mastitis intervention and serve as a basis for other infectious diseases.
first_indexed 2024-04-10T09:45:17Z
format Article
id doaj.art-5414e23df68a4bedb2f66c57bb22c8f0
institution Directory Open Access Journal
issn 1553-7366
1553-7374
language English
last_indexed 2024-04-10T09:45:17Z
publishDate 2023-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj.art-5414e23df68a4bedb2f66c57bb22c8f02023-02-17T05:31:49ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742023-01-01191e101110810.1371/journal.ppat.1011108A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.Caijun ZhaoLijuan BaoYihong ZhaoKeyi WuMin QiuLianjun FengNaisheng ZhangXiaoyu HuYunhe FuMounting evidence suggests that the gut microbiota plays an important role in the pathogenesis of mastitis, an important disease affecting the health of lactating women and the development of the dairy industry. However, the effect of the regulation of the gut microbiota by dietary components on mastitis development remains unknown. In this study, we found that a fiber-enriched diet alleviated Staphylococcus aureus (S. au)-induced mastitis in mice, which was dependent on the gut microbiota as depletion of the gut microbiota by antibiotics abolished this protective effect. Likewise, fecal microbiota transplantation (FMT) from high-inulin (HI)-treated mice (HIF) to recipient mice improved S. au-induced mastitis in mice. Consumption of an HI diet and HIF increased fecal short-chain fatty acid (SCFA) levels compared with the control group. Moreover, treatment with SCFAs, especially butyrate, alleviated S. au-induced mastitis in mice. Mechanistically, consumption of an HI diet enhanced the host antimicrobial program in macrophages through inhibiting histone deacetylase 3 by the production of butyrate. Collectively, our results suggest that modulation of the gut microbiota and its metabolism by dietary components is a potential strategy for mastitis intervention and serve as a basis for other infectious diseases.https://doi.org/10.1371/journal.ppat.1011108
spellingShingle Caijun Zhao
Lijuan Bao
Yihong Zhao
Keyi Wu
Min Qiu
Lianjun Feng
Naisheng Zhang
Xiaoyu Hu
Yunhe Fu
A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
PLoS Pathogens
title A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
title_full A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
title_fullStr A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
title_full_unstemmed A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
title_short A fiber-enriched diet alleviates Staphylococcus aureus-induced mastitis by activating the HDAC3-mediated antimicrobial program in macrophages via butyrate production in mice.
title_sort fiber enriched diet alleviates staphylococcus aureus induced mastitis by activating the hdac3 mediated antimicrobial program in macrophages via butyrate production in mice
url https://doi.org/10.1371/journal.ppat.1011108
work_keys_str_mv AT caijunzhao afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT lijuanbao afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT yihongzhao afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT keyiwu afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT minqiu afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT lianjunfeng afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT naishengzhang afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT xiaoyuhu afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT yunhefu afiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT caijunzhao fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT lijuanbao fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT yihongzhao fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT keyiwu fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT minqiu fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT lianjunfeng fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT naishengzhang fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT xiaoyuhu fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice
AT yunhefu fiberenricheddietalleviatesstaphylococcusaureusinducedmastitisbyactivatingthehdac3mediatedantimicrobialprograminmacrophagesviabutyrateproductioninmice