Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes

Abstract The emergence and rapid spread of antimicrobial resistance is of global public health concern. The gut microbiota harboring diverse commensal and opportunistic bacteria that can acquire resistance via horizontal and vertical gene transfers is considered an important reservoir and sink of an...

Full description

Bibliographic Details
Main Authors: Yuhao Fu, Qingyuan Dou, Kornelia Smalla, Yu Wang, Timothy A. Johnson, Kristian K. Brandt, Zhi Mei, Maoyuan Liao, Syed A. Hashsham, Andreas Schäffer, Hauke Smidt, Tong Zhang, Hui Li, Robert Stedtfeld, Hongjie Sheng, Benli Chai, Marko Virta, Xin Jiang, Fang Wang, Yong‐Guan Zhu, James M. Tiedje
Format: Article
Language:English
Published: Wiley 2023-12-01
Series:mLife
Subjects:
Online Access:https://doi.org/10.1002/mlf2.12101
_version_ 1797372381299212288
author Yuhao Fu
Qingyuan Dou
Kornelia Smalla
Yu Wang
Timothy A. Johnson
Kristian K. Brandt
Zhi Mei
Maoyuan Liao
Syed A. Hashsham
Andreas Schäffer
Hauke Smidt
Tong Zhang
Hui Li
Robert Stedtfeld
Hongjie Sheng
Benli Chai
Marko Virta
Xin Jiang
Fang Wang
Yong‐Guan Zhu
James M. Tiedje
author_facet Yuhao Fu
Qingyuan Dou
Kornelia Smalla
Yu Wang
Timothy A. Johnson
Kristian K. Brandt
Zhi Mei
Maoyuan Liao
Syed A. Hashsham
Andreas Schäffer
Hauke Smidt
Tong Zhang
Hui Li
Robert Stedtfeld
Hongjie Sheng
Benli Chai
Marko Virta
Xin Jiang
Fang Wang
Yong‐Guan Zhu
James M. Tiedje
author_sort Yuhao Fu
collection DOAJ
description Abstract The emergence and rapid spread of antimicrobial resistance is of global public health concern. The gut microbiota harboring diverse commensal and opportunistic bacteria that can acquire resistance via horizontal and vertical gene transfers is considered an important reservoir and sink of antibiotic resistance genes (ARGs). In this review, we describe the reservoirs of gut ARGs and their dynamics in both animals and humans, use the One Health perspective to track the transmission of ARG‐containing bacteria between humans, animals, and the environment, and assess the impact of antimicrobial resistance on human health and socioeconomic development. The gut resistome can evolve in an environment subject to various selective pressures, including antibiotic administration and environmental and lifestyle factors (e.g., diet, age, gender, and living conditions), and interventions through probiotics. Strategies to reduce the abundance of clinically relevant antibiotic‐resistant bacteria and their resistance determinants in various environmental niches are needed to ensure the mitigation of acquired antibiotic resistance. With the help of effective measures taken at the national, local, personal, and intestinal management, it will also result in preventing or minimizing the spread of infectious diseases. This review aims to improve our understanding of the correlations between intestinal microbiota and antimicrobial resistance and provide a basis for the development of management strategies to mitigate the antimicrobial resistance crisis.
first_indexed 2024-03-08T18:33:50Z
format Article
id doaj.art-937af0719be049469640f99e188805a3
institution Directory Open Access Journal
issn 2770-100X
language English
last_indexed 2024-03-08T18:33:50Z
publishDate 2023-12-01
publisher Wiley
record_format Article
series mLife
spelling doaj.art-937af0719be049469640f99e188805a32023-12-29T16:36:04ZengWileymLife2770-100X2023-12-012435036410.1002/mlf2.12101Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomesYuhao Fu0Qingyuan Dou1Kornelia Smalla2Yu Wang3Timothy A. Johnson4Kristian K. Brandt5Zhi Mei6Maoyuan Liao7Syed A. Hashsham8Andreas Schäffer9Hauke Smidt10Tong Zhang11Hui Li12Robert Stedtfeld13Hongjie Sheng14Benli Chai15Marko Virta16Xin Jiang17Fang Wang18Yong‐Guan Zhu19James M. Tiedje20State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaJulius Kühn Institute (JKI) Federal Research Centre for Cultivated Plants Braunschweig GermanyState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaDepartment of Animal Sciences Purdue University West Lafayette Indiana USASection for Microbial Ecology and Biotechnology, Department of Plant and Environmental Sciences University of Copenhagen Frederiksberg C DenmarkState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaDepartment of Plant, Soil and Microbial Sciences, Center for Microbial Ecology Michigan State University Michigan USAInstitute for Environmental Research RWTH Aachen University Aachen GermanyLaboratory of Microbiology Wageningen University & Research Wageningen The NetherlandsEnvironmental Microbiome Engineering and Biotechnology Laboratory, Center for Environmental Engineering Research, Department of Civil Engineering The University of Hong Kong Pokfulam Hong Kong ChinaDepartment of Plant, Soil and Microbial Sciences, Center for Microbial Ecology Michigan State University Michigan USADepartment of Civil and Environmental Engineering Michigan State University Michigan USAInstitute of Agricultural Resources and Environment Jiangsu Academy of Agricultural Sciences Nanjing ChinaDepartment of Plant, Soil and Microbial Sciences, Center for Microbial Ecology Michigan State University Michigan USADepartment of Microbiology University of Helsinki Helsinki FinlandState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaUniversity of Chinese Academy of Sciences Beijing ChinaDepartment of Plant, Soil and Microbial Sciences, Center for Microbial Ecology Michigan State University Michigan USAAbstract The emergence and rapid spread of antimicrobial resistance is of global public health concern. The gut microbiota harboring diverse commensal and opportunistic bacteria that can acquire resistance via horizontal and vertical gene transfers is considered an important reservoir and sink of antibiotic resistance genes (ARGs). In this review, we describe the reservoirs of gut ARGs and their dynamics in both animals and humans, use the One Health perspective to track the transmission of ARG‐containing bacteria between humans, animals, and the environment, and assess the impact of antimicrobial resistance on human health and socioeconomic development. The gut resistome can evolve in an environment subject to various selective pressures, including antibiotic administration and environmental and lifestyle factors (e.g., diet, age, gender, and living conditions), and interventions through probiotics. Strategies to reduce the abundance of clinically relevant antibiotic‐resistant bacteria and their resistance determinants in various environmental niches are needed to ensure the mitigation of acquired antibiotic resistance. With the help of effective measures taken at the national, local, personal, and intestinal management, it will also result in preventing or minimizing the spread of infectious diseases. This review aims to improve our understanding of the correlations between intestinal microbiota and antimicrobial resistance and provide a basis for the development of management strategies to mitigate the antimicrobial resistance crisis.https://doi.org/10.1002/mlf2.12101antibioticantimicrobial resistancegut microbiotamodulatory strategiesOne Health
spellingShingle Yuhao Fu
Qingyuan Dou
Kornelia Smalla
Yu Wang
Timothy A. Johnson
Kristian K. Brandt
Zhi Mei
Maoyuan Liao
Syed A. Hashsham
Andreas Schäffer
Hauke Smidt
Tong Zhang
Hui Li
Robert Stedtfeld
Hongjie Sheng
Benli Chai
Marko Virta
Xin Jiang
Fang Wang
Yong‐Guan Zhu
James M. Tiedje
Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
mLife
antibiotic
antimicrobial resistance
gut microbiota
modulatory strategies
One Health
title Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
title_full Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
title_fullStr Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
title_full_unstemmed Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
title_short Gut microbiota research nexus: One Health relationship between human, animal, and environmental resistomes
title_sort gut microbiota research nexus one health relationship between human animal and environmental resistomes
topic antibiotic
antimicrobial resistance
gut microbiota
modulatory strategies
One Health
url https://doi.org/10.1002/mlf2.12101
work_keys_str_mv AT yuhaofu gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT qingyuandou gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT korneliasmalla gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT yuwang gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT timothyajohnson gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT kristiankbrandt gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT zhimei gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT maoyuanliao gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT syedahashsham gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT andreasschaffer gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT haukesmidt gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT tongzhang gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT huili gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT robertstedtfeld gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT hongjiesheng gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT benlichai gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT markovirta gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT xinjiang gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT fangwang gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT yongguanzhu gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes
AT jamesmtiedje gutmicrobiotaresearchnexusonehealthrelationshipbetweenhumananimalandenvironmentalresistomes