Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide

Peter J. Diebold, Matthew W. Rhee, Qiaojuan Shi, Nguyen Vinh Trung, Fayaz Umrani, Sheraz Ahmed, Vandana Kulkarni, Prasad Deshpande, Mallika Alexander, Ngo Hoa, Nicholas A. Christakis, Najeeha Talat Iqbal, Syed Asad Ali, Jyoti S. Mathad and Ilana L. Brito ()
Additional contact information
Peter J. Diebold: Cornell University
Matthew W. Rhee: Cornell University
Qiaojuan Shi: Cornell University
Nguyen Vinh Trung: Oxford University Clinical Research Unit (OUCRU) in Ho Chi Minh City
Fayaz Umrani: Aga Khan University
Sheraz Ahmed: Aga Khan University
Vandana Kulkarni: Johns Hopkins University Clinical Trials Unit, Byramjee Jeejeebhoy Government Medical College
Prasad Deshpande: Johns Hopkins University Clinical Trials Unit, Byramjee Jeejeebhoy Government Medical College
Mallika Alexander: Johns Hopkins University Clinical Trials Unit, Byramjee Jeejeebhoy Government Medical College
Ngo Hoa: Oxford University Clinical Research Unit (OUCRU) in Ho Chi Minh City
Nicholas A. Christakis: Yale University
Najeeha Talat Iqbal: Aga Khan University
Syed Asad Ali: Aga Khan University
Jyoti S. Mathad: Weill Cornell Medicine
Ilana L. Brito: Cornell University

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract The acquisition of antimicrobial resistance (AR) genes has rendered important pathogens nearly or fully unresponsive to antibiotics. It has been suggested that pathogens acquire AR traits from the gut microbiota, which collectively serve as a global reservoir for AR genes conferring resistance to all classes of antibiotics. However, only a subset of AR genes confers resistance to clinically relevant antibiotics, and, although these AR gene profiles are well-characterized for common pathogens, less is known about their taxonomic associations and transfer potential within diverse members of the gut microbiota. We examined a collection of 14,850 human metagenomes and 1666 environmental metagenomes from 33 countries, in addition to nearly 600,000 isolate genomes, to gain insight into the global prevalence and taxonomic range of clinically relevant AR genes. We find that several of the most concerning AR genes, such as those encoding the cephalosporinase CTX-M and carbapenemases KPC, IMP, NDM, and VIM, remain taxonomically restricted to Proteobacteria. Even cfiA, the most common carbapenemase gene within the human gut microbiome, remains tightly restricted to Bacteroides, despite being found on a mobilizable plasmid. We confirmed these findings in gut microbiome samples from India, Honduras, Pakistan, and Vietnam, using a high-sensitivity single-cell fusion PCR approach. Focusing on a set of genes encoding carbapenemases and cephalosporinases, thus far restricted to Bacteroides species, we find that few mutations are required for efficacy in a different phylum, raising the question of why these genes have not spread more widely. Overall, these data suggest that globally prevalent, clinically relevant AR genes have not yet established themselves across diverse commensal gut microbiota.

Date: 2023
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DOI: 10.1038/s41467-023-42998-6

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