Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes
Soil represents a significant reservoir of antibiotic resistance genes (ARGs), which can potentially spread across distinct ecosystems and be acquired by pathogens threatening human as well as animal health. Currently, information on the identity and diversity of these genes, enabling anticipation o...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00460/full |
| _version_ | 1818518581682372608 |
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| author | Inka Marie Willms Aysha Kamran Nils Frederik Aßmann Denis Krone Simon Henning Bolz Fabian Fiedler Heiko Nacke |
| author_facet | Inka Marie Willms Aysha Kamran Nils Frederik Aßmann Denis Krone Simon Henning Bolz Fabian Fiedler Heiko Nacke |
| author_sort | Inka Marie Willms |
| collection | DOAJ |
| description | Soil represents a significant reservoir of antibiotic resistance genes (ARGs), which can potentially spread across distinct ecosystems and be acquired by pathogens threatening human as well as animal health. Currently, information on the identity and diversity of these genes, enabling anticipation of possible future resistance development in clinical environments and the livestock sector, is lacking. In this study, we applied functional metagenomics to discover novel sulfonamide as well as tetracycline resistance genes in soils derived from forest and grassland. Screening of soil metagenomic libraries revealed a total of eight so far unknown ARGs. The recovered genes originate from phylogenetically diverse soil bacteria (e.g., Actinobacteria, Chloroflexi, or Proteobacteria) and encode proteins with a minimum identity of 46% to other antibiotic resistance determinants. In particular forest soil ecosystems have so far been neglected in studies focusing on antibiotic resistance. Here, we detected for the first time non-mobile dihydropteroate synthase (DHPS) genes conferring resistance to sulfonamides in forest soil with no history of exposure to these synthetic drugs. In total, three sulfonamide resistant DHPSs, differing in taxonomic origin, were discovered in beech or pine forest soil. This indicates that sulfonamide resistance naturally occurs in forest-resident soil bacterial communities. Besides forest soil-derived sulfonamide resistance proteins, we also identified a DHPS affiliated to Chloroflexi in grassland soil. This enzyme and the other recovered DHPSs confer reduced susceptibility toward sulfamethazine, which is widely used in food animal production. With respect to tetracycline resistance, four efflux proteins affiliated to the major facilitator superfamily (MFS) were identified. Noteworthy, one of these proteins also conferred reduced susceptibility toward lincomycin. |
| first_indexed | 2024-12-11T01:12:04Z |
| format | Article |
| id | doaj.art-c45a755e9da8425cb7b46915f57e14c8 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-11T01:12:04Z |
| publishDate | 2019-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-c45a755e9da8425cb7b46915f57e14c82022-12-22T01:26:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-03-011010.3389/fmicb.2019.00460441731Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil MetagenomesInka Marie Willms0Aysha Kamran1Nils Frederik Aßmann2Denis Krone3Simon Henning Bolz4Fabian Fiedler5Heiko Nacke6Department of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of General Microbiology, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanyDepartment of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University, Göttingen, GermanySoil represents a significant reservoir of antibiotic resistance genes (ARGs), which can potentially spread across distinct ecosystems and be acquired by pathogens threatening human as well as animal health. Currently, information on the identity and diversity of these genes, enabling anticipation of possible future resistance development in clinical environments and the livestock sector, is lacking. In this study, we applied functional metagenomics to discover novel sulfonamide as well as tetracycline resistance genes in soils derived from forest and grassland. Screening of soil metagenomic libraries revealed a total of eight so far unknown ARGs. The recovered genes originate from phylogenetically diverse soil bacteria (e.g., Actinobacteria, Chloroflexi, or Proteobacteria) and encode proteins with a minimum identity of 46% to other antibiotic resistance determinants. In particular forest soil ecosystems have so far been neglected in studies focusing on antibiotic resistance. Here, we detected for the first time non-mobile dihydropteroate synthase (DHPS) genes conferring resistance to sulfonamides in forest soil with no history of exposure to these synthetic drugs. In total, three sulfonamide resistant DHPSs, differing in taxonomic origin, were discovered in beech or pine forest soil. This indicates that sulfonamide resistance naturally occurs in forest-resident soil bacterial communities. Besides forest soil-derived sulfonamide resistance proteins, we also identified a DHPS affiliated to Chloroflexi in grassland soil. This enzyme and the other recovered DHPSs confer reduced susceptibility toward sulfamethazine, which is widely used in food animal production. With respect to tetracycline resistance, four efflux proteins affiliated to the major facilitator superfamily (MFS) were identified. Noteworthy, one of these proteins also conferred reduced susceptibility toward lincomycin.https://www.frontiersin.org/article/10.3389/fmicb.2019.00460/fullsoil metagenomefunctional metagenomicsantibiotic resistancedihydropteroate synthasetetracycline resistancesulfonamide resistance |
| spellingShingle | Inka Marie Willms Aysha Kamran Nils Frederik Aßmann Denis Krone Simon Henning Bolz Fabian Fiedler Heiko Nacke Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes Frontiers in Microbiology soil metagenome functional metagenomics antibiotic resistance dihydropteroate synthase tetracycline resistance sulfonamide resistance |
| title | Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes |
| title_full | Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes |
| title_fullStr | Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes |
| title_full_unstemmed | Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes |
| title_short | Discovery of Novel Antibiotic Resistance Determinants in Forest and Grassland Soil Metagenomes |
| title_sort | discovery of novel antibiotic resistance determinants in forest and grassland soil metagenomes |
| topic | soil metagenome functional metagenomics antibiotic resistance dihydropteroate synthase tetracycline resistance sulfonamide resistance |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00460/full |
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