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Resistome Analysis of Global Livestock and Soil Microbiomes

Antimicrobial resistance (AMR) is a serious threat to public health globally; it is estimated that AMR bacteria caused 1.27 million deaths in 2019, and this is set to rise to 10 million deaths annually. Agricultural and soil environments act as antimicrobial resistance gene (ARG) reservoirs, operati...

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Autores principales: Lawther, Katie, Santos, Fernanda Godoy, Oyama, Linda Boniface, Rubino, Francesco, Morrison, Steven, Creevey, Chris J., McGrath, John W., Huws, Sharon Ann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9300982/
https://www.ncbi.nlm.nih.gov/pubmed/35875563
http://dx.doi.org/10.3389/fmicb.2022.897905
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author Lawther, Katie
Santos, Fernanda Godoy
Oyama, Linda Boniface
Rubino, Francesco
Morrison, Steven
Creevey, Chris J.
McGrath, John W.
Huws, Sharon Ann
author_facet Lawther, Katie
Santos, Fernanda Godoy
Oyama, Linda Boniface
Rubino, Francesco
Morrison, Steven
Creevey, Chris J.
McGrath, John W.
Huws, Sharon Ann
author_sort Lawther, Katie
collection PubMed
description Antimicrobial resistance (AMR) is a serious threat to public health globally; it is estimated that AMR bacteria caused 1.27 million deaths in 2019, and this is set to rise to 10 million deaths annually. Agricultural and soil environments act as antimicrobial resistance gene (ARG) reservoirs, operating as a link between different ecosystems and enabling the mixing and dissemination of resistance genes. Due to the close interactions between humans and agricultural environments, these AMR gene reservoirs are a major risk to both human and animal health. In this study, we aimed to identify the resistance gene reservoirs present in four microbiomes: poultry, ruminant, swine gastrointestinal (GI) tracts coupled with those from soil. This large study brings together every poultry, swine, ruminant, and soil shotgun metagenomic sequence available on the NCBI sequence read archive for the first time. We use the ResFinder database to identify acquired antimicrobial resistance genes in over 5,800 metagenomes. ARGs were diverse and widespread within the metagenomes, with 235, 101, 167, and 182 different resistance genes identified in the poultry, ruminant, swine, and soil microbiomes, respectively. The tetracycline resistance genes were the most widespread in the livestock GI microbiomes, including tet(W)_1, tet(Q)_1, tet(O)_1, and tet(44)_1. The tet(W)_1 resistance gene was found in 99% of livestock GI tract microbiomes, while tet(Q)_1 was identified in 93%, tet(O)_1 in 82%, and finally tet(44)_1 in 69%. Metatranscriptomic analysis confirmed these genes were “real” and expressed in one or more of the livestock GI tract microbiomes, with tet(40)_1 and tet(O)_1 expressed in all three livestock microbiomes. In soil, the most abundant ARG was the oleandomycin resistance gene, ole(B)_1. A total of 55 resistance genes were shared by the four microbiomes, with 11 ARGs actively expressed in two or more microbiomes. By using all available metagenomes we were able to mine a large number of samples and describe resistomes in 37 countries. This study provides a global insight into the diverse and abundant antimicrobial resistance gene reservoirs present in both livestock and soil microbiomes.
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spelling pubmed-93009822022-07-22 Resistome Analysis of Global Livestock and Soil Microbiomes Lawther, Katie Santos, Fernanda Godoy Oyama, Linda Boniface Rubino, Francesco Morrison, Steven Creevey, Chris J. McGrath, John W. Huws, Sharon Ann Front Microbiol Microbiology Antimicrobial resistance (AMR) is a serious threat to public health globally; it is estimated that AMR bacteria caused 1.27 million deaths in 2019, and this is set to rise to 10 million deaths annually. Agricultural and soil environments act as antimicrobial resistance gene (ARG) reservoirs, operating as a link between different ecosystems and enabling the mixing and dissemination of resistance genes. Due to the close interactions between humans and agricultural environments, these AMR gene reservoirs are a major risk to both human and animal health. In this study, we aimed to identify the resistance gene reservoirs present in four microbiomes: poultry, ruminant, swine gastrointestinal (GI) tracts coupled with those from soil. This large study brings together every poultry, swine, ruminant, and soil shotgun metagenomic sequence available on the NCBI sequence read archive for the first time. We use the ResFinder database to identify acquired antimicrobial resistance genes in over 5,800 metagenomes. ARGs were diverse and widespread within the metagenomes, with 235, 101, 167, and 182 different resistance genes identified in the poultry, ruminant, swine, and soil microbiomes, respectively. The tetracycline resistance genes were the most widespread in the livestock GI microbiomes, including tet(W)_1, tet(Q)_1, tet(O)_1, and tet(44)_1. The tet(W)_1 resistance gene was found in 99% of livestock GI tract microbiomes, while tet(Q)_1 was identified in 93%, tet(O)_1 in 82%, and finally tet(44)_1 in 69%. Metatranscriptomic analysis confirmed these genes were “real” and expressed in one or more of the livestock GI tract microbiomes, with tet(40)_1 and tet(O)_1 expressed in all three livestock microbiomes. In soil, the most abundant ARG was the oleandomycin resistance gene, ole(B)_1. A total of 55 resistance genes were shared by the four microbiomes, with 11 ARGs actively expressed in two or more microbiomes. By using all available metagenomes we were able to mine a large number of samples and describe resistomes in 37 countries. This study provides a global insight into the diverse and abundant antimicrobial resistance gene reservoirs present in both livestock and soil microbiomes. Frontiers Media S.A. 2022-07-07 /pmc/articles/PMC9300982/ /pubmed/35875563 http://dx.doi.org/10.3389/fmicb.2022.897905 Text en Copyright © 2022 Lawther, Santos, Oyama, Rubino, Morrison, Creevey, McGrath and Huws. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Lawther, Katie
Santos, Fernanda Godoy
Oyama, Linda Boniface
Rubino, Francesco
Morrison, Steven
Creevey, Chris J.
McGrath, John W.
Huws, Sharon Ann
Resistome Analysis of Global Livestock and Soil Microbiomes
title Resistome Analysis of Global Livestock and Soil Microbiomes
title_full Resistome Analysis of Global Livestock and Soil Microbiomes
title_fullStr Resistome Analysis of Global Livestock and Soil Microbiomes
title_full_unstemmed Resistome Analysis of Global Livestock and Soil Microbiomes
title_short Resistome Analysis of Global Livestock and Soil Microbiomes
title_sort resistome analysis of global livestock and soil microbiomes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9300982/
https://www.ncbi.nlm.nih.gov/pubmed/35875563
http://dx.doi.org/10.3389/fmicb.2022.897905
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