Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria
Abstract Soil is an important reservoir of antibiotic resistance genes (ARGs) and understanding how corresponding environmental changes influence their emergence, evolution, and spread is crucial. The soil-dwelling bacterial genus Listeria, including L. monocytogenes, the causative agent of listerio...
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Nature Portfolio
2024-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54459-9 |
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| author | Ying-Xian Goh Sai Manohar Balu Anupoju Anthony Nguyen Hailong Zhang Monica Ponder Leigh-Anne Krometis Amy Pruden Jingqiu Liao |
| author_facet | Ying-Xian Goh Sai Manohar Balu Anupoju Anthony Nguyen Hailong Zhang Monica Ponder Leigh-Anne Krometis Amy Pruden Jingqiu Liao |
| author_sort | Ying-Xian Goh |
| collection | DOAJ |
| description | Abstract Soil is an important reservoir of antibiotic resistance genes (ARGs) and understanding how corresponding environmental changes influence their emergence, evolution, and spread is crucial. The soil-dwelling bacterial genus Listeria, including L. monocytogenes, the causative agent of listeriosis, serves as a key model for establishing this understanding. Here, we characterize ARGs in 594 genomes representing 19 Listeria species that we previously isolated from soils in natural environments across the United States. Among the five putatively functional ARGs identified, lin, which confers resistance to lincomycin, is the most prevalent, followed by mprF, sul, fosX, and norB. ARGs are predominantly found in Listeria sensu stricto species, with those more closely related to L. monocytogenes tending to harbor more ARGs. Notably, phylogenetic and recombination analyses provide evidence of recent horizontal gene transfer (HGT) in all five ARGs within and/or across species, likely mediated by transformation rather than conjugation and transduction. In addition, the richness and genetic divergence of ARGs are associated with environmental conditions, particularly soil properties (e.g., aluminum and magnesium) and surrounding land use patterns (e.g., forest coverage). Collectively, our data suggest that recent HGT and environmental selection play a vital role in the acquisition and diversification of bacterial ARGs in natural environments. |
| format | Article |
| id | doaj-art-c2d6d4e63a8e4d4f8bdb80f9dd43c4e7 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
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| series | Nature Communications |
| spelling | doaj-art-c2d6d4e63a8e4d4f8bdb80f9dd43c4e72024-11-24T12:34:20ZengNature PortfolioNature Communications2041-17232024-11-0115111310.1038/s41467-024-54459-9Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling ListeriaYing-Xian Goh0Sai Manohar Balu Anupoju1Anthony Nguyen2Hailong Zhang3Monica Ponder4Leigh-Anne Krometis5Amy Pruden6Jingqiu Liao7Department of Civil and Environmental Engineering, Virginia TechDepartment of Computer Science, Virginia TechComputational Modeling & Data Analytics Program, Virginia TechDepartment of Business Information Technology, Virginia TechCenter for Emerging, Zoonotic, and Arthropod-Borne Pathogens, Virginia TechCenter for Emerging, Zoonotic, and Arthropod-Borne Pathogens, Virginia TechDepartment of Civil and Environmental Engineering, Virginia TechDepartment of Civil and Environmental Engineering, Virginia TechAbstract Soil is an important reservoir of antibiotic resistance genes (ARGs) and understanding how corresponding environmental changes influence their emergence, evolution, and spread is crucial. The soil-dwelling bacterial genus Listeria, including L. monocytogenes, the causative agent of listeriosis, serves as a key model for establishing this understanding. Here, we characterize ARGs in 594 genomes representing 19 Listeria species that we previously isolated from soils in natural environments across the United States. Among the five putatively functional ARGs identified, lin, which confers resistance to lincomycin, is the most prevalent, followed by mprF, sul, fosX, and norB. ARGs are predominantly found in Listeria sensu stricto species, with those more closely related to L. monocytogenes tending to harbor more ARGs. Notably, phylogenetic and recombination analyses provide evidence of recent horizontal gene transfer (HGT) in all five ARGs within and/or across species, likely mediated by transformation rather than conjugation and transduction. In addition, the richness and genetic divergence of ARGs are associated with environmental conditions, particularly soil properties (e.g., aluminum and magnesium) and surrounding land use patterns (e.g., forest coverage). Collectively, our data suggest that recent HGT and environmental selection play a vital role in the acquisition and diversification of bacterial ARGs in natural environments.https://doi.org/10.1038/s41467-024-54459-9 |
| spellingShingle | Ying-Xian Goh Sai Manohar Balu Anupoju Anthony Nguyen Hailong Zhang Monica Ponder Leigh-Anne Krometis Amy Pruden Jingqiu Liao Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria Nature Communications |
| title | Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria |
| title_full | Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria |
| title_fullStr | Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria |
| title_full_unstemmed | Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria |
| title_short | Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria |
| title_sort | evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil dwelling listeria |
| url | https://doi.org/10.1038/s41467-024-54459-9 |
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