Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment
The microbial ecosystem residing in the human gut is believed to play an important role in horizontal exchange of virulence and antibiotic resistance genes that threatens human health. While the diversity of gut-microorganisms and their genetic content has been studied extensively, high-resolution i...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01852/full |
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| author | Heidi Gumpert Heidi Gumpert Jessica Z. Kubicek-Sutherland Andreas Porse Nahid Karami Christian Munck Marius Linkevicius Ingegerd Adlerberth Agnes E. Wold Dan I. Andersson Morten O. A. Sommer |
| author_facet | Heidi Gumpert Heidi Gumpert Jessica Z. Kubicek-Sutherland Andreas Porse Nahid Karami Christian Munck Marius Linkevicius Ingegerd Adlerberth Agnes E. Wold Dan I. Andersson Morten O. A. Sommer |
| author_sort | Heidi Gumpert |
| collection | DOAJ |
| description | The microbial ecosystem residing in the human gut is believed to play an important role in horizontal exchange of virulence and antibiotic resistance genes that threatens human health. While the diversity of gut-microorganisms and their genetic content has been studied extensively, high-resolution insight into the plasticity, and selective forces shaping individual genomes is scarce. In a longitudinal study, we followed the dynamics of co-existing Escherichia coli lineages in an infant not receiving antibiotics. Using whole genome sequencing, we observed large genomic deletions, bacteriophage infections, as well as the loss and acquisition of plasmids in these lineages during their colonization of the human gut. In particular, we captured the exchange of multidrug resistance genes, and identified a clinically relevant conjugative plasmid mediating the transfer. This resistant transconjugant lineage was maintained for months, demonstrating that antibiotic resistance genes can disseminate and persist in the gut microbiome; even in absence of antibiotic selection. Furthermore, through in vivo competition assays, we suggest that the resistant transconjugant can persist through a fitness advantage in the mouse gut in spite of a fitness cost in vitro. Our findings highlight the dynamic nature of the human gut microbiota and provide the first genomic description of antibiotic resistance gene transfer between bacteria in the unperturbed human gut. These results exemplify that conjugative plasmids, harboring resistance determinants, can transfer and persists in the gut in the absence of antibiotic treatment. |
| first_indexed | 2024-12-19T15:25:51Z |
| format | Article |
| id | doaj.art-b7b42f204bf449bd85aa7b8a3b80592a |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-19T15:25:51Z |
| publishDate | 2017-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-b7b42f204bf449bd85aa7b8a3b80592a2022-12-21T20:15:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-09-01810.3389/fmicb.2017.01852298526Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic TreatmentHeidi Gumpert0Heidi Gumpert1Jessica Z. Kubicek-Sutherland2Andreas Porse3Nahid Karami4Christian Munck5Marius Linkevicius6Ingegerd Adlerberth7Agnes E. Wold8Dan I. Andersson9Morten O. A. Sommer10Department of Systems Biology, Technical University of Denmark, Lyngby, DenmarkDepartment of Clinical Microbiology, Hvidovre Hospital, University of Copenhagen, Hvidovre, DenmarkDepartment of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, SwedenThe Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkDepartment of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenThe Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkDepartment of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, SwedenDepartment of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenDepartment of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenDepartment of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, SwedenThe Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkThe microbial ecosystem residing in the human gut is believed to play an important role in horizontal exchange of virulence and antibiotic resistance genes that threatens human health. While the diversity of gut-microorganisms and their genetic content has been studied extensively, high-resolution insight into the plasticity, and selective forces shaping individual genomes is scarce. In a longitudinal study, we followed the dynamics of co-existing Escherichia coli lineages in an infant not receiving antibiotics. Using whole genome sequencing, we observed large genomic deletions, bacteriophage infections, as well as the loss and acquisition of plasmids in these lineages during their colonization of the human gut. In particular, we captured the exchange of multidrug resistance genes, and identified a clinically relevant conjugative plasmid mediating the transfer. This resistant transconjugant lineage was maintained for months, demonstrating that antibiotic resistance genes can disseminate and persist in the gut microbiome; even in absence of antibiotic selection. Furthermore, through in vivo competition assays, we suggest that the resistant transconjugant can persist through a fitness advantage in the mouse gut in spite of a fitness cost in vitro. Our findings highlight the dynamic nature of the human gut microbiota and provide the first genomic description of antibiotic resistance gene transfer between bacteria in the unperturbed human gut. These results exemplify that conjugative plasmids, harboring resistance determinants, can transfer and persists in the gut in the absence of antibiotic treatment.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01852/fullEscherichia colihorizontal gene transferinfant gutgenome dynamicsplasmid transferin vivo fitness |
| spellingShingle | Heidi Gumpert Heidi Gumpert Jessica Z. Kubicek-Sutherland Andreas Porse Nahid Karami Christian Munck Marius Linkevicius Ingegerd Adlerberth Agnes E. Wold Dan I. Andersson Morten O. A. Sommer Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment Frontiers in Microbiology Escherichia coli horizontal gene transfer infant gut genome dynamics plasmid transfer in vivo fitness |
| title | Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment |
| title_full | Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment |
| title_fullStr | Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment |
| title_full_unstemmed | Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment |
| title_short | Transfer and Persistence of a Multi-Drug Resistance Plasmid in situ of the Infant Gut Microbiota in the Absence of Antibiotic Treatment |
| title_sort | transfer and persistence of a multi drug resistance plasmid in situ of the infant gut microbiota in the absence of antibiotic treatment |
| topic | Escherichia coli horizontal gene transfer infant gut genome dynamics plasmid transfer in vivo fitness |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01852/full |
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