The resistome of European coastal environments revealed by high-resolution targeted metagenomics in oysters
8 affiliations
- 1Department of Earth, Environmental, and Life Sciences, University of Genoa, Genoa, 16132 Italy
- 2IHPE, Université de Montpellier, CNRS, IFREMER, Université de Perpignan Via Domitia, Place Eugène Bataillon, Montpellier, 34090 France
- 3Department of Surgical Sciences and Integrated Diagnostics (DISC), University of Genoa, Genoa, Italy
- 4Laboratoire Des Sciences de L’Environnement MARin (LEMAR), Université de Brest, IFREMER, CNRS, IRD, Rue Dumont D’urville, Plouzané, 29280 France
- 5IFREMER, Unité Physiologie Fonctionnelle Des Organismes Marins, ZI de La Pointe du Diable, Plouzané, 29280 France
- 6Molecular Ecology Group (MEG), Water Research Institute, National Research Council of Italy (CNR-IRSA), Verbania, Italy
- 7Institute of Agrifood Research and Technology (IRTA), Aquaculture Program, La Ràpita, Tarragona, Spain
- 8Alfred Wegener Institute–Helmholtz Centre for Polar and Marine Research, Wadden Sea Station Sylt, List, Germany
Abstract
Background: Antimicrobial resistance is a major global health threat, and the environment is increasingly recognised as a key reservoir of antibiotic resistance genes (ARGs). In marine ecosystems, filter-feeding organisms such as oysters are sentinel species that reflect the microbiological diversity of their environment. Here, we investigated the ARG content of the Pacific oyster Magallana gigas across four European coastal sites, contrasting anthropogenically impacted aquaculture sites (Bay of Brest, Ebro Delta, Thau lagoon) with natural oyster reefs (Sylt island). ARGs sequencing was enriched using a targeted probe-and-capture metagenomic approach employing 37,826 RNA baits covering over 2000 ARG sequences. Moreover, a novel bioinformatic pipeline ARGifier was specifically designed for sensitive, high-resolution detection and classification of ARGs in metagenomic samples dominated by host DNA.
Results: This strategy was able to overcome limitations of cultivation-based methods and whole metagenomic sequencing, enabling the detection of more than 33,000 ARG sequences in the oyster resistome spanning over 450 genes distributed over 23 resistance classes. Reads assigned to ARGs represented 0.23% of all raw reads and 25.02% of host-depleted reads. Accordingly, comparison of targeted metagenomics and pool-seq analysis of cultured isolates (culturomics) in specific pathogen-free oysters revealed that metagenomics captured dominant, community-wide resistance determinants, whereas culturomics recovered a broader diversity of ARGs due to their presence in genomes of cultivable strains. The oyster resistome across the four farming sites was dominated by multidrug efflux systems associated with intrinsic and housekeeping-related mechanisms, suggesting an environmentally shaped resistance profile. Clinically relevant ARGs, including extended-spectrum Beta-Lactamase, carbapenem, colistin, and vancomycin resistance genes, were detected in low abundance at all sites, with higher enrichment in anthropogenically impacted areas. In addition, several ARGs were associated with plasmids, indicating mobilization potential. Taxonomic analysis revealed that a limited subset of bacteria, particularly Betaproteobacteria and Actinomycetes, carried a disproportionately high number of ARGs despite their low relative abundance in the oyster microbiome.
Conclusions: Overall, this study delivers a comprehensive inventory of ecologically and clinically relevant ARGs in European coastal environments, positioning farmed and wild oysters as sentinel organisms for monitoring antimicrobial resistance in coastal waters. Our findings highlight the circulation of ARGs within coastal marine ecosystems, which may act as reservoirs and potential sources of mobilisable antimicrobial resistance.
Video Abstract
Supplementary Information: The online version contains supplementary material available at https://doi.org/10.1186/s40168-026-02485-8.
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BibTeX
@article{auguste2026resistome,
title = {{The resistome of European coastal environments revealed by high-resolution targeted metagenomics in oysters}},
author = {Manon Auguste and Emanuele Bosi and Jamal Saad and Caterina Oliveri and Lapo Doni and Anna Marchese and Marie-Agnès Travers and Eve Toulza and Viviane Boulo and Gaelle Courtay and Bruno Petton and Hugo Koechlin and Caroline Montagnani and Andrea Di Cesare and Gianluca Corno and Karl B. Andree and Ignasi Gairin and Dolors Furones and Coralie Broquard and K. Mathias Wegner and Delphine Destoumieux-Garzón and Luigi Vezzulli},
journal = {Microbiome},
year = {2026},
month = jul,
doi = {10.1186/s40168-026-02485-8},
url = {https://hal.science/hal-05785890v1},
note = {CC BY-NC-ND 4.0},
}
RIS
TY - JOUR
TI - The resistome of European coastal environments revealed by high-resolution targeted metagenomics in oysters
AU - Manon Auguste
AU - Emanuele Bosi
AU - Jamal Saad
AU - Caterina Oliveri
AU - Lapo Doni
AU - Anna Marchese
AU - Marie-Agnès Travers
AU - Eve Toulza
AU - Viviane Boulo
AU - Gaelle Courtay
AU - Bruno Petton
AU - Hugo Koechlin
AU - Caroline Montagnani
AU - Andrea Di Cesare
AU - Gianluca Corno
AU - Karl B. Andree
AU - Ignasi Gairin
AU - Dolors Furones
AU - Coralie Broquard
AU - K. Mathias Wegner
AU - Delphine Destoumieux-Garzón
AU - Luigi Vezzulli
PY - 2026
DA - 2026/07/28
JO - Microbiome
DO - 10.1186/s40168-026-02485-8
UR - https://hal.science/hal-05785890v1
AB - Background: Antimicrobial resistance is a major global health threat, and the environment is increasingly recognised as a key reservoir of antibiotic resistance genes (ARGs). In marine ecosystems, filter-feeding organisms such as oysters are sentinel species that reflect the microbiological diversity of their environment. Here, we investigated the ARG content of the Pacific oyster Magallana gigas across four European coastal sites, contrasting anthropogenically impacted aquaculture sites (Bay of Brest, Ebro Delta, Thau lagoon) with natural oyster reefs (Sylt island). ARGs sequencing was enriched using a targeted probe-and-capture metagenomic approach employing 37,826 RNA baits covering over 2000 ARG sequences. Moreover, a novel bioinformatic pipeline ARGifier was specifically designed for sensitive, high-resolution detection and classification of ARGs in metagenomic samples dominated by host DNA. Results: This strategy was able to overcome limitations of cultivation-based methods and whole metagenomic sequencing, enabling the detection of more than 33,000 ARG sequences in the oyster resistome spanning over 450 genes distributed over 23 resistance classes. Reads assigned to ARGs represented 0.23% of all raw reads and 25.02% of host-depleted reads. Accordingly, comparison of targeted metagenomics and pool-seq analysis of cultured isolates (culturomics) in specific pathogen-free oysters revealed that metagenomics captured dominant, community-wide resistance determinants, whereas culturomics recovered a broader diversity of ARGs due to their presence in genomes of cultivable strains. The oyster resistome across the four farming sites was dominated by multidrug efflux systems associated with intrinsic and housekeeping-related mechanisms, suggesting an environmentally shaped resistance profile. Clinically relevant ARGs, including extended-spectrum Beta-Lactamase, carbapenem, colistin, and vancomycin resistance genes, were detected in low abundance at all sites, with higher enrichment in anthropogenically impacted areas. In addition, several ARGs were associated with plasmids, indicating mobilization potential. Taxonomic analysis revealed that a limited subset of bacteria, particularly Betaproteobacteria and Actinomycetes, carried a disproportionately high number of ARGs despite their low relative abundance in the oyster microbiome. Conclusions: Overall, this study delivers a comprehensive inventory of ecologically and clinically relevant ARGs in European coastal environments, positioning farmed and wild oysters as sentinel organisms for monitoring antimicrobial resistance in coastal waters. Our findings highlight the circulation of ARGs within coastal marine ecosystems, which may act as reservoirs and potential sources of mobilisable antimicrobial resistance. Video Abstract Supplementary Information: The online version contains supplementary material available at https://doi.org/10.1186/s40168-026-02485-8.
SN - 2049-2618
ER -