Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages

Extensive use of antibiotics in human healthcare as well as in agricultural and environmental settings has led to the emergence and spread of antibiotic-resistant bacteria, rendering many infections increasingly difficult to treat. Coupled with the limited development of new antibiotics, the rise of...

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Main Authors: Nikoline S. Olsen, Leise Riber
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/14/3/296
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author Nikoline S. Olsen
Leise Riber
author_facet Nikoline S. Olsen
Leise Riber
author_sort Nikoline S. Olsen
collection DOAJ
description Extensive use of antibiotics in human healthcare as well as in agricultural and environmental settings has led to the emergence and spread of antibiotic-resistant bacteria, rendering many infections increasingly difficult to treat. Coupled with the limited development of new antibiotics, the rise of antimicrobial resistance (AMR) has caused a major health crisis worldwide, which calls for immediate action. Strengthening AMR surveillance systems is, therefore, crucial to global and national efforts in combating this escalating threat. This review explores the potential of metagenomics, a sequenced-based approach to analyze entire microbial communities without the need for cultivation, as a transformative and rapid tool for improving AMR surveillance strategies as compared to traditional cultivation-based methods. We emphasize the importance of monitoring mobile genetic elements (MGEs), such as integrons, transposons, plasmids, and bacteriophages (phages), in relation to their critical role in facilitating the dissemination of genetic resistance determinants via horizontal gene transfer (HGT) across diverse environments and clinical settings. In this context, the strengths and limitations of current bioinformatic tools designed to detect AMR-associated MGEs in metagenomic datasets, including the emerging potential of predictive machine learning models, are evaluated. Moreover, the controversial role of phages in AMR transmission is discussed alongside the potential of phage therapy as a promising alternative to conventional antibiotic treatment.
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spelling doaj-art-dc48ca5f10c947adba98a6ede5b8a4e72025-08-20T02:42:38ZengMDPI AGAntibiotics2079-63822025-03-0114329610.3390/antibiotics14030296Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of PhagesNikoline S. Olsen0Leise Riber1Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg, DenmarkDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg, DenmarkExtensive use of antibiotics in human healthcare as well as in agricultural and environmental settings has led to the emergence and spread of antibiotic-resistant bacteria, rendering many infections increasingly difficult to treat. Coupled with the limited development of new antibiotics, the rise of antimicrobial resistance (AMR) has caused a major health crisis worldwide, which calls for immediate action. Strengthening AMR surveillance systems is, therefore, crucial to global and national efforts in combating this escalating threat. This review explores the potential of metagenomics, a sequenced-based approach to analyze entire microbial communities without the need for cultivation, as a transformative and rapid tool for improving AMR surveillance strategies as compared to traditional cultivation-based methods. We emphasize the importance of monitoring mobile genetic elements (MGEs), such as integrons, transposons, plasmids, and bacteriophages (phages), in relation to their critical role in facilitating the dissemination of genetic resistance determinants via horizontal gene transfer (HGT) across diverse environments and clinical settings. In this context, the strengths and limitations of current bioinformatic tools designed to detect AMR-associated MGEs in metagenomic datasets, including the emerging potential of predictive machine learning models, are evaluated. Moreover, the controversial role of phages in AMR transmission is discussed alongside the potential of phage therapy as a promising alternative to conventional antibiotic treatment.https://www.mdpi.com/2079-6382/14/3/296antimicrobial resistance (AMR)antibiotic resistance genes (ARGs)surveillancemetagenomicsmobile genetic elements (MGEs)plasmids
spellingShingle Nikoline S. Olsen
Leise Riber
Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
Antibiotics
antimicrobial resistance (AMR)
antibiotic resistance genes (ARGs)
surveillance
metagenomics
mobile genetic elements (MGEs)
plasmids
title Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
title_full Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
title_fullStr Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
title_full_unstemmed Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
title_short Metagenomics as a Transformative Tool for Antibiotic Resistance Surveillance: Highlighting the Impact of Mobile Genetic Elements with a Focus on the Complex Role of Phages
title_sort metagenomics as a transformative tool for antibiotic resistance surveillance highlighting the impact of mobile genetic elements with a focus on the complex role of phages
topic antimicrobial resistance (AMR)
antibiotic resistance genes (ARGs)
surveillance
metagenomics
mobile genetic elements (MGEs)
plasmids
url https://www.mdpi.com/2079-6382/14/3/296
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