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Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility
The spread of antibiotic resistance genes (ARGs) that are present in livestock manures, which are discharged into the environment, is a severe threat to human and animal health. Here, we used 16S rRNA gene profiling and metagenomic analysis to characterize microbial community composition and antibio...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692488/ https://www.ncbi.nlm.nih.gov/pubmed/36422370 http://dx.doi.org/10.3390/microorganisms10112301 |
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author | Begmatov, Shahjahon Beletsky, Alexey V. Gruzdev, Eugeny V. Mardanov, Andrey V. Glukhova, Lubov B. Karnachuk, Olga V. Ravin, Nikolai V. |
author_facet | Begmatov, Shahjahon Beletsky, Alexey V. Gruzdev, Eugeny V. Mardanov, Andrey V. Glukhova, Lubov B. Karnachuk, Olga V. Ravin, Nikolai V. |
author_sort | Begmatov, Shahjahon |
collection | PubMed |
description | The spread of antibiotic resistance genes (ARGs) that are present in livestock manures, which are discharged into the environment, is a severe threat to human and animal health. Here, we used 16S rRNA gene profiling and metagenomic analysis to characterize microbial community composition and antibiotic resistance in a manure storage lagoon from a large-scale swine finishing facility. Manure samples were collected at intervals of two years. Both the prokaryotic community and the resistome were dominated by the Firmicutes, Proteobacteria and Bacteroidota. Metagenomic analysis of two samples revealed 726 and 641 ARGs classified into 59 and 46 AMR gene families. Besides multidrug efflux pumps, the predominating ARGs potentially encoded resistance to tetracyclines, macrolide–lincosamide–streptogramin, aminoglycosides, peptide antibiotics, rifamycin, chloramphenicol, and beta-lactams. Genes from all predominant AMR gene families were found in both samples indicating overall long-term stability of the resistome. Antibiotic efflux pumps were the primary type of ARGs in the Proteobacteria, while antibiotic target alteration or protection was the main mechanism of resistance in the Firmicutes, Actinobacteriota and Bacteroidota. Metagenome-assembled genomes (MAG) of four multidrug-resistant strains were assembled. The first MAG, assigned to Escherichia flexneri, contained 46 ARGs, including multidrug efflux pumps, modified porins, beta-lactamases, and genes conferring resistance to peptide antibiotics. The second MAG, assigned to the family Alcaligenaceae, contained 18 ARGs encoding resistance to macrolide–lincosamide–streptogramin, tetracyclines, aminoglycosides and diaminopyrimidins. Two other MAGs representing the genera Atopostipes and Prevotella, contained four and seven ARGs, respectively. All these MAGs represented minor community members and accounted for less than 0.3% of the whole metagenome. Overall, a few lineages originated from the gut but relatively rare in the manure storage lagoon, are the main source of ARGs and some of them carry multiple resistance determinants. |
format | Online Article Text |
id | pubmed-9692488 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-96924882022-11-26 Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility Begmatov, Shahjahon Beletsky, Alexey V. Gruzdev, Eugeny V. Mardanov, Andrey V. Glukhova, Lubov B. Karnachuk, Olga V. Ravin, Nikolai V. Microorganisms Article The spread of antibiotic resistance genes (ARGs) that are present in livestock manures, which are discharged into the environment, is a severe threat to human and animal health. Here, we used 16S rRNA gene profiling and metagenomic analysis to characterize microbial community composition and antibiotic resistance in a manure storage lagoon from a large-scale swine finishing facility. Manure samples were collected at intervals of two years. Both the prokaryotic community and the resistome were dominated by the Firmicutes, Proteobacteria and Bacteroidota. Metagenomic analysis of two samples revealed 726 and 641 ARGs classified into 59 and 46 AMR gene families. Besides multidrug efflux pumps, the predominating ARGs potentially encoded resistance to tetracyclines, macrolide–lincosamide–streptogramin, aminoglycosides, peptide antibiotics, rifamycin, chloramphenicol, and beta-lactams. Genes from all predominant AMR gene families were found in both samples indicating overall long-term stability of the resistome. Antibiotic efflux pumps were the primary type of ARGs in the Proteobacteria, while antibiotic target alteration or protection was the main mechanism of resistance in the Firmicutes, Actinobacteriota and Bacteroidota. Metagenome-assembled genomes (MAG) of four multidrug-resistant strains were assembled. The first MAG, assigned to Escherichia flexneri, contained 46 ARGs, including multidrug efflux pumps, modified porins, beta-lactamases, and genes conferring resistance to peptide antibiotics. The second MAG, assigned to the family Alcaligenaceae, contained 18 ARGs encoding resistance to macrolide–lincosamide–streptogramin, tetracyclines, aminoglycosides and diaminopyrimidins. Two other MAGs representing the genera Atopostipes and Prevotella, contained four and seven ARGs, respectively. All these MAGs represented minor community members and accounted for less than 0.3% of the whole metagenome. Overall, a few lineages originated from the gut but relatively rare in the manure storage lagoon, are the main source of ARGs and some of them carry multiple resistance determinants. MDPI 2022-11-20 /pmc/articles/PMC9692488/ /pubmed/36422370 http://dx.doi.org/10.3390/microorganisms10112301 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Begmatov, Shahjahon Beletsky, Alexey V. Gruzdev, Eugeny V. Mardanov, Andrey V. Glukhova, Lubov B. Karnachuk, Olga V. Ravin, Nikolai V. Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title | Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title_full | Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title_fullStr | Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title_full_unstemmed | Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title_short | Distribution Patterns of Antibiotic Resistance Genes and Their Bacterial Hosts in a Manure Lagoon of a Large-Scale Swine Finishing Facility |
title_sort | distribution patterns of antibiotic resistance genes and their bacterial hosts in a manure lagoon of a large-scale swine finishing facility |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692488/ https://www.ncbi.nlm.nih.gov/pubmed/36422370 http://dx.doi.org/10.3390/microorganisms10112301 |
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