Characterization of antibiotic resistomes by reprogrammed bacteriophage-enabled functional metagenomics in clinical strains

Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. He...

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Published inNature microbiology Vol. 8; no. 3; pp. 410 - 423
Main Authors Apjok, Gábor, Számel, Mónika, Christodoulou, Chryso, Seregi, Viktória, Vásárhelyi, Bálint Márk, Stirling, Tamás, Eszenyi, Bálint, Sári, Tóbiás, Vidovics, Fanni, Nagrand, Erika, Kovács, Dorina, Szili, Petra, Lantos, Ildikó Ilona, Méhi, Orsolya, Jangir, Pramod K, Herczeg, Róbert, Gálik, Bence, Urbán, Péter, Gyenesei, Attila, Draskovits, Gábor, Nyerges, Ákos, Fekete, Gergely, Bodai, László, Zsindely, Nóra, Dénes, Béla, Yosef, Ido, Qimron, Udi, Papp, Balázs, Pál, Csaba, Kintses, Bálint
Format Journal Article
LanguageEnglish
Published England Nature Publishing Group 01.03.2023
Nature Publishing Group UK
Subjects
Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Antibiotics
Bacteria
Bacteria - genetics
Bacteriophages - genetics
Drug resistance
Genes, Bacterial
Genomes
Host specificity
Intestinal microflora
Metagenomics
Microbiomes
Phages
Site-directed mutagenesis
Species
Strains (organisms)
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Abstract Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. Here we present a functional metagenomics pipeline called Reprogrammed Bacteriophage Particle Assisted Multi-species Functional Metagenomics (DEEPMINE). This approach combines and improves the use of T7 bacteriophage with exchanged tail fibres and targeted mutagenesis to expand phage host-specificity and efficiency for functional metagenomics. These modified phage particles were used to introduce large metagenomic plasmid libraries into clinically relevant bacterial pathogens. By screening for ARGs in soil and gut microbiomes and clinical genomes against 13 antibiotics, we demonstrate that this approach substantially expands the list of identified ARGs. Many ARGs have species-specific effects on resistance; they provide a high level of resistance in one bacterial species but yield very limited resistance in a related species. Finally, we identified mobile ARGs against antibiotics that are currently under clinical development or have recently been approved. Overall, DEEPMINE expands the functional metagenomics toolbox for studying microbial communities.
AbstractList Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. Here we present a functional metagenomics pipeline called Reprogrammed Bacteriophage Particle Assisted Multi-species Functional Metagenomics (DEEPMINE). This approach combines and improves the use of T7 bacteriophage with exchanged tail fibres and targeted mutagenesis to expand phage host-specificity and efficiency for functional metagenomics. These modified phage particles were used to introduce large metagenomic plasmid libraries into clinically relevant bacterial pathogens. By screening for ARGs in soil and gut microbiomes and clinical genomes against 13 antibiotics, we demonstrate that this approach substantially expands the list of identified ARGs. Many ARGs have species-specific effects on resistance; they provide a high level of resistance in one bacterial species but yield very limited resistance in a related species. Finally, we identified mobile ARGs against antibiotics that are currently under clinical development or have recently been approved. Overall, DEEPMINE expands the functional metagenomics toolbox for studying microbial communities. Application of reprogrammed bacteriophage to functional metagenomics in clinically relevant bacterial strains improves identification of antibiotic resistance genes, including those against recently developed or approved antibiotics.
Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. Here we present a functional metagenomics pipeline called Reprogrammed Bacteriophage Particle Assisted Multi-species Functional Metagenomics (DEEPMINE). This approach combines and improves the use of T7 bacteriophage with exchanged tail fibres and targeted mutagenesis to expand phage host-specificity and efficiency for functional metagenomics. These modified phage particles were used to introduce large metagenomic plasmid libraries into clinically relevant bacterial pathogens. By screening for ARGs in soil and gut microbiomes and clinical genomes against 13 antibiotics, we demonstrate that this approach substantially expands the list of identified ARGs. Many ARGs have species-specific effects on resistance; they provide a high level of resistance in one bacterial species but yield very limited resistance in a related species. Finally, we identified mobile ARGs against antibiotics that are currently under clinical development or have recently been approved. Overall, DEEPMINE expands the functional metagenomics toolbox for studying microbial communities.Application of reprogrammed bacteriophage to functional metagenomics in clinically relevant bacterial strains improves identification of antibiotic resistance genes, including those against recently developed or approved antibiotics.
Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. Here we present a functional metagenomics pipeline called Reprogrammed Bacteriophage Particle Assisted Multi-species Functional Metagenomics (DEEPMINE). This approach combines and improves the use of T7 bacteriophage with exchanged tail fibres and targeted mutagenesis to expand phage host-specificity and efficiency for functional metagenomics. These modified phage particles were used to introduce large metagenomic plasmid libraries into clinically relevant bacterial pathogens. By screening for ARGs in soil and gut microbiomes and clinical genomes against 13 antibiotics, we demonstrate that this approach substantially expands the list of identified ARGs. Many ARGs have species-specific effects on resistance; they provide a high level of resistance in one bacterial species but yield very limited resistance in a related species. Finally, we identified mobile ARGs against antibiotics that are currently under clinical development or have recently been approved. Overall, DEEPMINE expands the functional metagenomics toolbox for studying microbial communities.
Abstract Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host bacterial species is limited. This limitation affects both the scope of the identified ARGs and the interpretation of their clinical relevance. Here we present a functional metagenomics pipeline called Reprogrammed Bacteriophage Particle Assisted Multi-species Functional Metagenomics (DEEPMINE). This approach combines and improves the use of T7 bacteriophage with exchanged tail fibres and targeted mutagenesis to expand phage host-specificity and efficiency for functional metagenomics. These modified phage particles were used to introduce large metagenomic plasmid libraries into clinically relevant bacterial pathogens. By screening for ARGs in soil and gut microbiomes and clinical genomes against 13 antibiotics, we demonstrate that this approach substantially expands the list of identified ARGs. Many ARGs have species-specific effects on resistance; they provide a high level of resistance in one bacterial species but yield very limited resistance in a related species. Finally, we identified mobile ARGs against antibiotics that are currently under clinical development or have recently been approved. Overall, DEEPMINE expands the functional metagenomics toolbox for studying microbial communities.
Author Kovács, Dorina
Méhi, Orsolya
Qimron, Udi
Fekete, Gergely
Stirling, Tamás
Számel, Mónika
Nagrand, Erika
Herczeg, Róbert
Nyerges, Ákos
Christodoulou, Chryso
Urbán, Péter
Dénes, Béla
Kintses, Bálint
Zsindely, Nóra
Vidovics, Fanni
Szili, Petra
Jangir, Pramod K
Gálik, Bence
Pál, Csaba
Seregi, Viktória
Gyenesei, Attila
Sári, Tóbiás
Papp, Balázs
Eszenyi, Bálint
Draskovits, Gábor
Lantos, Ildikó Ilona
Vásárhelyi, Bálint Márk
Apjok, Gábor
Yosef, Ido
Bodai, László
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Publisher Nature Publishing Group
Nature Publishing Group UK
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Snippet Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable host...
Abstract Functional metagenomics is a powerful experimental tool to identify antibiotic resistance genes (ARGs) in the environment, but the range of suitable...
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proquest
crossref
pubmed
SourceType Open Access Repository
Aggregation Database
Index Database
StartPage 410
SubjectTerms Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Antibiotics
Bacteria
Bacteria - genetics
Bacteriophages - genetics
Drug resistance
Genes, Bacterial
Genomes
Host specificity
Intestinal microflora
Metagenomics
Microbiomes
Phages
Site-directed mutagenesis
Species
Strains (organisms)
Title Characterization of antibiotic resistomes by reprogrammed bacteriophage-enabled functional metagenomics in clinical strains
URI https://www.ncbi.nlm.nih.gov/pubmed/36759752
https://www.proquest.com/docview/2781418878/abstract/
https://search.proquest.com/docview/2775624031
https://pubmed.ncbi.nlm.nih.gov/PMC9981461
Volume 8
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