Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics
Abstract Antimicrobial resistance (AMR) poses a significant threat to global health. The indiscriminate use of antibiotics has accelerated the emergence and spread of drug-resistant bacteria, compromising our ability to treat infectious diseases. A One Health approach is essential to address this ur...
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Nature Portfolio
2025-04-01
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| Online Access: | https://doi.org/10.1038/s41598-025-90777-8 |
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| author | Rajindra Napit Anupama Gurung Ajit Poudel Ashok Chaudhary Prajwol Manandhar Ajay Narayan Sharma Samita Raut Saman Man Pradhan Jyotsna Joshi Mathilde Poyet Mathieu Groussin Rajesh M. Rajbhandari Dibesh B. Karmacharya |
| author_facet | Rajindra Napit Anupama Gurung Ajit Poudel Ashok Chaudhary Prajwol Manandhar Ajay Narayan Sharma Samita Raut Saman Man Pradhan Jyotsna Joshi Mathilde Poyet Mathieu Groussin Rajesh M. Rajbhandari Dibesh B. Karmacharya |
| author_sort | Rajindra Napit |
| collection | DOAJ |
| description | Abstract Antimicrobial resistance (AMR) poses a significant threat to global health. The indiscriminate use of antibiotics has accelerated the emergence and spread of drug-resistant bacteria, compromising our ability to treat infectious diseases. A One Health approach is essential to address this urgent issue, recognizing the interconnectedness of human, animal, and environmental health. This study investigated the prevalence and transmission of AMR in a temporary settlement in Kathmandu, Nepal. By employing shotgun metagenomics, we analyzed a diverse range of samples, including human fecal samples, avian fecal samples, and environmental samples. Our analysis revealed a complex interplay of pathogenic bacteria, virulence factors (VF), and antimicrobial resistance genes (ARGs) across these different domains. We identified a diverse range of bacterial species, including potential pathogens, in both human and animal samples. Notably, Prevotella spp. was the dominant gut bacterium in human samples. Additionally, we detected a wide range of phages and viruses, including Stx-2 converting phages, which can contribute to the virulence of Shiga toxin-producing E. coli (STEC) strains. Our analysis revealed the presence of 72 virulence factor genes and 53 ARG subtypes across the studied samples. Poultry samples exhibited the highest number of ARG subtypes, suggesting that the intensive use of antibiotics in poultry production may contribute to the dissemination of AMR. Furthermore, we observed frequent horizontal gene transfer (HGT) events, with gut microbiomes serving as key reservoirs for ARGs. This study underscores the critical role of a One Health approach in addressing AMR. By integrating human, animal, and environmental health perspectives, we can better understand the complex dynamics of AMR and develop effective strategies for prevention and control. Our findings highlight the urgent need for robust surveillance systems, judicious antibiotic use, and improved hygiene practices to mitigate the impact of AMR on public health. |
| format | Article |
| id | doaj-art-567119dd5f4d48d09f2a9013d6523577 |
| institution | DOAJ |
| issn | 2045-2322 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj-art-567119dd5f4d48d09f2a9013d65235772025-08-20T02:39:24ZengNature PortfolioScientific Reports2045-23222025-04-0115111510.1038/s41598-025-90777-8Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamicsRajindra Napit0Anupama Gurung1Ajit Poudel2Ashok Chaudhary3Prajwol Manandhar4Ajay Narayan Sharma5Samita Raut6Saman Man Pradhan7Jyotsna Joshi8Mathilde Poyet9Mathieu Groussin10Rajesh M. Rajbhandari11Dibesh B. Karmacharya12Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Dept. of Biological Engineering, Massachusetts Institute of TechnologyDept. of Biological Engineering, Massachusetts Institute of TechnologyCenter for Molecular Dynamics Nepal (CMDN)Center for Molecular Dynamics Nepal (CMDN)Abstract Antimicrobial resistance (AMR) poses a significant threat to global health. The indiscriminate use of antibiotics has accelerated the emergence and spread of drug-resistant bacteria, compromising our ability to treat infectious diseases. A One Health approach is essential to address this urgent issue, recognizing the interconnectedness of human, animal, and environmental health. This study investigated the prevalence and transmission of AMR in a temporary settlement in Kathmandu, Nepal. By employing shotgun metagenomics, we analyzed a diverse range of samples, including human fecal samples, avian fecal samples, and environmental samples. Our analysis revealed a complex interplay of pathogenic bacteria, virulence factors (VF), and antimicrobial resistance genes (ARGs) across these different domains. We identified a diverse range of bacterial species, including potential pathogens, in both human and animal samples. Notably, Prevotella spp. was the dominant gut bacterium in human samples. Additionally, we detected a wide range of phages and viruses, including Stx-2 converting phages, which can contribute to the virulence of Shiga toxin-producing E. coli (STEC) strains. Our analysis revealed the presence of 72 virulence factor genes and 53 ARG subtypes across the studied samples. Poultry samples exhibited the highest number of ARG subtypes, suggesting that the intensive use of antibiotics in poultry production may contribute to the dissemination of AMR. Furthermore, we observed frequent horizontal gene transfer (HGT) events, with gut microbiomes serving as key reservoirs for ARGs. This study underscores the critical role of a One Health approach in addressing AMR. By integrating human, animal, and environmental health perspectives, we can better understand the complex dynamics of AMR and develop effective strategies for prevention and control. Our findings highlight the urgent need for robust surveillance systems, judicious antibiotic use, and improved hygiene practices to mitigate the impact of AMR on public health.https://doi.org/10.1038/s41598-025-90777-8Antimicrobial resistanceAntimicrobial resistance genesGut microbiomeHorizontal gene transferOne health |
| spellingShingle | Rajindra Napit Anupama Gurung Ajit Poudel Ashok Chaudhary Prajwol Manandhar Ajay Narayan Sharma Samita Raut Saman Man Pradhan Jyotsna Joshi Mathilde Poyet Mathieu Groussin Rajesh M. Rajbhandari Dibesh B. Karmacharya Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics Scientific Reports Antimicrobial resistance Antimicrobial resistance genes Gut microbiome Horizontal gene transfer One health |
| title | Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics |
| title_full | Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics |
| title_fullStr | Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics |
| title_full_unstemmed | Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics |
| title_short | Metagenomic analysis of human, animal, and environmental samples identifies potential emerging pathogens, profiles antibiotic resistance genes, and reveals horizontal gene transfer dynamics |
| title_sort | metagenomic analysis of human animal and environmental samples identifies potential emerging pathogens profiles antibiotic resistance genes and reveals horizontal gene transfer dynamics |
| topic | Antimicrobial resistance Antimicrobial resistance genes Gut microbiome Horizontal gene transfer One health |
| url | https://doi.org/10.1038/s41598-025-90777-8 |
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