Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters
Abstract Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARG...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2022-01-01
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| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-021-00260-1 |
| _version_ | 1830209203932758016 |
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| author | Wei Yan A. Brantley Hall Xiaofang Jiang |
| author_facet | Wei Yan A. Brantley Hall Xiaofang Jiang |
| author_sort | Wei Yan |
| collection | DOAJ |
| description | Abstract Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARGs regulated by invertible promoters remains poorly understood. Here, we sought to assess the threat posed by ARGs regulated by invertible promoters by systematically searching for ARGs regulated by invertible promoters in the human gut microbiome and examining their origin, prevalence, and distribution. Through metagenomic assembly of 2227 human gut metagenomes and genomic analysis of the Unified Human Gastrointestinal Genome (UHGG) collection, we identified ARGs regulated by invertible promoters and categorized them into three classes based on the invertase-regulating phase variation. In the human gut microbiome, ARGs regulated by invertible promoters are exclusively found in Bacteroidales species. Through genomic analysis, we observed that ARGs regulated by invertible promoters have convergently originated from ARG insertions into glycan-synthesis loci that were regulated by invertible promoters at least three times. Moreover, all three classes of invertible promoters regulating ARGs are located within integrative conjugative elements (ICEs). Therefore, horizontal transfer via ICEs could explain the wide taxonomic distribution of ARGs regulated by invertible promoters. Overall, these findings reveal that glycan-synthesis loci regulated by invertible promoters in Bacteroidales species are an important hotspot for the emergence of clinically-relevant ARGs regulated by invertible promoters. |
| first_indexed | 2024-12-18T05:03:05Z |
| format | Article |
| id | doaj.art-514f87ddf37147a3905db026f8277513 |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-12-18T05:03:05Z |
| publishDate | 2022-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-514f87ddf37147a3905db026f82775132022-12-21T21:20:05ZengNature Portfolionpj Biofilms and Microbiomes2055-50082022-01-01811910.1038/s41522-021-00260-1Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promotersWei Yan0A. Brantley Hall1Xiaofang Jiang2National Library of Medicine, National Institutes of HealthDepartment of Cell Biology and Molecular Genetics, University of MarylandNational Library of Medicine, National Institutes of HealthAbstract Antibiotic-resistance genes (ARGs) regulated by invertible promoters can mitigate the fitness cost of maintaining ARGs in the absence of antibiotics and could potentially prolong the persistence of ARGs in bacterial populations. However, the origin, prevalence, and distribution of these ARGs regulated by invertible promoters remains poorly understood. Here, we sought to assess the threat posed by ARGs regulated by invertible promoters by systematically searching for ARGs regulated by invertible promoters in the human gut microbiome and examining their origin, prevalence, and distribution. Through metagenomic assembly of 2227 human gut metagenomes and genomic analysis of the Unified Human Gastrointestinal Genome (UHGG) collection, we identified ARGs regulated by invertible promoters and categorized them into three classes based on the invertase-regulating phase variation. In the human gut microbiome, ARGs regulated by invertible promoters are exclusively found in Bacteroidales species. Through genomic analysis, we observed that ARGs regulated by invertible promoters have convergently originated from ARG insertions into glycan-synthesis loci that were regulated by invertible promoters at least three times. Moreover, all three classes of invertible promoters regulating ARGs are located within integrative conjugative elements (ICEs). Therefore, horizontal transfer via ICEs could explain the wide taxonomic distribution of ARGs regulated by invertible promoters. Overall, these findings reveal that glycan-synthesis loci regulated by invertible promoters in Bacteroidales species are an important hotspot for the emergence of clinically-relevant ARGs regulated by invertible promoters.https://doi.org/10.1038/s41522-021-00260-1 |
| spellingShingle | Wei Yan A. Brantley Hall Xiaofang Jiang Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters npj Biofilms and Microbiomes |
| title | Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| title_full | Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| title_fullStr | Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| title_full_unstemmed | Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| title_short | Bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| title_sort | bacteroidales species in the human gut are a reservoir of antibiotic resistance genes regulated by invertible promoters |
| url | https://doi.org/10.1038/s41522-021-00260-1 |
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