Using genomics to explore the epidemiology of vancomycin resistance in a sewage system
ABSTRACT VanHAX-mediated glycopeptide resistance has been consistently high in one of the three main sewer systems in Copenhagen, Lynetten, for +20 years. To explore this for other glycopeptide resistance genes, and whether the colonization has resulted in establishment of multiple bacterial taxa, w...
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| Language: | English |
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American Society for Microbiology
2025-01-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01489-24 |
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| author | Emilie Egholm Bruun Jensen Saria Otani Ivan Liachko Benjamin Auch Frank M. Aarestrup |
| author_facet | Emilie Egholm Bruun Jensen Saria Otani Ivan Liachko Benjamin Auch Frank M. Aarestrup |
| author_sort | Emilie Egholm Bruun Jensen |
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| description | ABSTRACT VanHAX-mediated glycopeptide resistance has been consistently high in one of the three main sewer systems in Copenhagen, Lynetten, for +20 years. To explore this for other glycopeptide resistance genes, and whether the colonization has resulted in establishment of multiple bacterial taxa, we mapped 505 shotgun metagenomic data sets from the inlet of three sewage treatment plants to 831 different glycopeptide resistance genes. Only vanHAX and vanHBX genes were differentially abundant in Lynetten. Analyses of eight contigs suggested limited variations in the flanking regions. Proximity ligation metagenomic analysis of 12 samples from Lynetten identified 441 and 5 paired reads mapping to vanHAX and vanHBX, respectively. The other end of these reads was mapped to generated metagenomic-assembled genomes and NCBI using BLAST. vanHBX could only be linked to the phylum level (Bacillota). Plasmid analysis of vanHBX Hi-C contigs showed that these were mainly located on plasmids reported found in enterococci species. Most vanHAX-linked reads could only be linked to phylum and class level, but some reads were assigned to Enterococcus faecium (7 reads), Enterococcus faecalis (4 reads), Paenibacillus apiarius (2 reads), and Paenibacillus thiaminolyticus (27 reads). Ten of the 20 Hi-C contigs-containing vanHAX were annotated as plasmid, all reported found in Enterococcus species. This study shows that while Hi-C technology is valuable for linking antimicrobial resistance genes to bacterial taxa, it suffers from challenges in reliably mapping the linked read to a genomic region with sufficient taxonomic information. Our results also suggest that over the +20 years of colonizing a sewer system, vanHAX has not become widespread across multiple taxa, remaining primarily in E. faecalis and E. faecium, with the exception of Paenibacillus.IMPORTANCELong-term colonization of microbial communities with antimicrobial-resistant bacteria is expected to result in sharing of the resistance genes between several different bacterial taxa of the communities. We investigated microbiomes from a sewer, which have been colonized with glycopeptide-resistant bacteria harboring the mobile vanHAX gene cluster for a minimum of 20 years, using metagenomics sequencing and Hi-C. We found that despite the long-term presence in the sewer, the vanHAX genes have seemingly not disseminated widely. |
| format | Article |
| id | doaj-art-8258963f970c44378f1e5f9c03ee6086 |
| institution | Kabale University |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-8258963f970c44378f1e5f9c03ee60862025-01-07T14:05:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.01489-24Using genomics to explore the epidemiology of vancomycin resistance in a sewage systemEmilie Egholm Bruun Jensen0Saria Otani1Ivan Liachko2Benjamin Auch3Frank M. Aarestrup4National Food Institute, Technical University of Denmark, Kgs Lyngby, GhanaNational Food Institute, Technical University of Denmark, Kgs Lyngby, GhanaPhase Genomics, Seattle, Washington, USAPhase Genomics, Seattle, Washington, USANational Food Institute, Technical University of Denmark, Kgs Lyngby, GhanaABSTRACT VanHAX-mediated glycopeptide resistance has been consistently high in one of the three main sewer systems in Copenhagen, Lynetten, for +20 years. To explore this for other glycopeptide resistance genes, and whether the colonization has resulted in establishment of multiple bacterial taxa, we mapped 505 shotgun metagenomic data sets from the inlet of three sewage treatment plants to 831 different glycopeptide resistance genes. Only vanHAX and vanHBX genes were differentially abundant in Lynetten. Analyses of eight contigs suggested limited variations in the flanking regions. Proximity ligation metagenomic analysis of 12 samples from Lynetten identified 441 and 5 paired reads mapping to vanHAX and vanHBX, respectively. The other end of these reads was mapped to generated metagenomic-assembled genomes and NCBI using BLAST. vanHBX could only be linked to the phylum level (Bacillota). Plasmid analysis of vanHBX Hi-C contigs showed that these were mainly located on plasmids reported found in enterococci species. Most vanHAX-linked reads could only be linked to phylum and class level, but some reads were assigned to Enterococcus faecium (7 reads), Enterococcus faecalis (4 reads), Paenibacillus apiarius (2 reads), and Paenibacillus thiaminolyticus (27 reads). Ten of the 20 Hi-C contigs-containing vanHAX were annotated as plasmid, all reported found in Enterococcus species. This study shows that while Hi-C technology is valuable for linking antimicrobial resistance genes to bacterial taxa, it suffers from challenges in reliably mapping the linked read to a genomic region with sufficient taxonomic information. Our results also suggest that over the +20 years of colonizing a sewer system, vanHAX has not become widespread across multiple taxa, remaining primarily in E. faecalis and E. faecium, with the exception of Paenibacillus.IMPORTANCELong-term colonization of microbial communities with antimicrobial-resistant bacteria is expected to result in sharing of the resistance genes between several different bacterial taxa of the communities. We investigated microbiomes from a sewer, which have been colonized with glycopeptide-resistant bacteria harboring the mobile vanHAX gene cluster for a minimum of 20 years, using metagenomics sequencing and Hi-C. We found that despite the long-term presence in the sewer, the vanHAX genes have seemingly not disseminated widely.https://journals.asm.org/doi/10.1128/spectrum.01489-24Hi-Cmetagenomicsmetagenome assembliesantimicrobial resistancesewageglycopeptide resistance |
| spellingShingle | Emilie Egholm Bruun Jensen Saria Otani Ivan Liachko Benjamin Auch Frank M. Aarestrup Using genomics to explore the epidemiology of vancomycin resistance in a sewage system Microbiology Spectrum Hi-C metagenomics metagenome assemblies antimicrobial resistance sewage glycopeptide resistance |
| title | Using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| title_full | Using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| title_fullStr | Using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| title_full_unstemmed | Using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| title_short | Using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| title_sort | using genomics to explore the epidemiology of vancomycin resistance in a sewage system |
| topic | Hi-C metagenomics metagenome assemblies antimicrobial resistance sewage glycopeptide resistance |
| url | https://journals.asm.org/doi/10.1128/spectrum.01489-24 |
| work_keys_str_mv | AT emilieegholmbruunjensen usinggenomicstoexploretheepidemiologyofvancomycinresistanceinasewagesystem AT sariaotani usinggenomicstoexploretheepidemiologyofvancomycinresistanceinasewagesystem AT ivanliachko usinggenomicstoexploretheepidemiologyofvancomycinresistanceinasewagesystem AT benjaminauch usinggenomicstoexploretheepidemiologyofvancomycinresistanceinasewagesystem AT frankmaarestrup usinggenomicstoexploretheepidemiologyofvancomycinresistanceinasewagesystem |