Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis

Bovine digital dermatitis (DD) is a contagious infectious cause of lameness in cattle with unknown definitive etiologies. Many of the bacterial species detected in metagenomic analyses of DD lesions are difficult to culture, and their antimicrobial resistance status is largely unknown. Recently, a n...

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Main Authors: Ashenafi F. Beyi, Alan Hassall, Gregory J. Phillips, Paul J. Plummer
Format: Article
Language:English
Published: MDPI AG 2021-02-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/10/2/221
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author Ashenafi F. Beyi
Alan Hassall
Gregory J. Phillips
Paul J. Plummer
author_facet Ashenafi F. Beyi
Alan Hassall
Gregory J. Phillips
Paul J. Plummer
author_sort Ashenafi F. Beyi
collection DOAJ
description Bovine digital dermatitis (DD) is a contagious infectious cause of lameness in cattle with unknown definitive etiologies. Many of the bacterial species detected in metagenomic analyses of DD lesions are difficult to culture, and their antimicrobial resistance status is largely unknown. Recently, a novel proximity ligation-guided metagenomic approach (Hi-C ProxiMeta) has been used to identify bacterial reservoirs of antimicrobial resistance genes (ARGs) directly from microbial communities, without the need to culture individual bacteria. The objective of this study was to track tetracycline resistance determinants in bacteria involved in DD pathogenesis using Hi-C. A pooled sample of macerated tissues from clinical DD lesions was used for this purpose. Metagenome deconvolution using ProxiMeta resulted in the creation of 40 metagenome-assembled genomes with ≥80% complete genomes, classified into five phyla. Further, 1959 tetracycline resistance genes and ARGs conferring resistance to aminoglycoside, beta-lactams, sulfonamide, phenicol, lincosamide, and erythromycin were identified along with their bacterial hosts. In conclusion, the widespread distribution of genes conferring resistance against tetracycline and other antimicrobials in bacteria of DD lesions is reported for the first time. Use of proximity ligation to identify microorganisms hosting specific ARGs holds promise for tracking ARGs transmission in complex microbial communities.
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spelling doaj.art-1a2314858f4249ad8e9f1bbc431c48e92023-12-11T18:07:21ZengMDPI AGAntibiotics2079-63822021-02-0110222110.3390/antibiotics10020221Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital DermatitisAshenafi F. Beyi0Alan Hassall1Gregory J. Phillips2Paul J. Plummer3Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA 50011, USAVeterinary Diagnostic and Production Animal Medicine, Iowa State University, Ames, IA 50011, USAVeterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA 50011, USAVeterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA 50011, USABovine digital dermatitis (DD) is a contagious infectious cause of lameness in cattle with unknown definitive etiologies. Many of the bacterial species detected in metagenomic analyses of DD lesions are difficult to culture, and their antimicrobial resistance status is largely unknown. Recently, a novel proximity ligation-guided metagenomic approach (Hi-C ProxiMeta) has been used to identify bacterial reservoirs of antimicrobial resistance genes (ARGs) directly from microbial communities, without the need to culture individual bacteria. The objective of this study was to track tetracycline resistance determinants in bacteria involved in DD pathogenesis using Hi-C. A pooled sample of macerated tissues from clinical DD lesions was used for this purpose. Metagenome deconvolution using ProxiMeta resulted in the creation of 40 metagenome-assembled genomes with ≥80% complete genomes, classified into five phyla. Further, 1959 tetracycline resistance genes and ARGs conferring resistance to aminoglycoside, beta-lactams, sulfonamide, phenicol, lincosamide, and erythromycin were identified along with their bacterial hosts. In conclusion, the widespread distribution of genes conferring resistance against tetracycline and other antimicrobials in bacteria of DD lesions is reported for the first time. Use of proximity ligation to identify microorganisms hosting specific ARGs holds promise for tracking ARGs transmission in complex microbial communities.https://www.mdpi.com/2079-6382/10/2/221antimicrobial resistance genesdigital dermatitisHi-C ProxiMetaresistomestetracycline resistance
spellingShingle Ashenafi F. Beyi
Alan Hassall
Gregory J. Phillips
Paul J. Plummer
Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
Antibiotics
antimicrobial resistance genes
digital dermatitis
Hi-C ProxiMeta
resistomes
tetracycline resistance
title Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
title_full Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
title_fullStr Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
title_full_unstemmed Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
title_short Tracking Reservoirs of Antimicrobial Resistance Genes in a Complex Microbial Community Using Metagenomic Hi-C: The Case of Bovine Digital Dermatitis
title_sort tracking reservoirs of antimicrobial resistance genes in a complex microbial community using metagenomic hi c the case of bovine digital dermatitis
topic antimicrobial resistance genes
digital dermatitis
Hi-C ProxiMeta
resistomes
tetracycline resistance
url https://www.mdpi.com/2079-6382/10/2/221
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