Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics

[EN] Here, the role of the dairy-processing chain as a reservoir of antimicrobial resistance (AR) determinants and a source of novel biocontrol quorum-sensing inhibitors is assessed through a functional metagenomics approach. A metagenomic library comprising ~22,000 recombinant clones was built from...

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Autores: Alexa, Elena-Alexandra, Walsh, Calum J., Coughlan, Laura M., Awad, Amal, Simon, Cezara A., Ruiz, Lorena, Crispie, Fiona, Cotter, Paul D., Álvarez Ordóñez, Avelino
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Universidad de León
Repositorio:BULERIA. Repositorio Institucional de la Universidad de León
OAI Identifier:oai:buleria.unileon.es:10612/21012
Acceso en línea:https://journals.asm.org/doi/10.1128/msystems.00723-19
https://hdl.handle.net/10612/21012
Access Level:acceso abierto
Palabra clave:Tecnología de los alimentos
Antibiotic resistance
Food safety
Functional metagenomics
Dairy products
Quorum quenching
3309 Tecnología de Los Alimentos
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spelling Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional MetagenomicsAlexa, Elena-AlexandraWalsh, Calum J.Coughlan, Laura M.Awad, AmalSimon, Cezara A.Ruiz, LorenaCrispie, FionaCotter, Paul D.Álvarez Ordóñez, AvelinoTecnología de los alimentosAntibiotic resistanceFood safetyFunctional metagenomicsDairy productsQuorum quenching3309 Tecnología de Los Alimentos[EN] Here, the role of the dairy-processing chain as a reservoir of antimicrobial resistance (AR) determinants and a source of novel biocontrol quorum-sensing inhibitors is assessed through a functional metagenomics approach. A metagenomic library comprising ~22,000 recombinant clones was built from DNA isolated from raw milk, raw milk cheeses, and cheese-processing environment swab samples. The high-throughput sequencing of 9,216 recombinant clones showed that lactic acid bacteria (LAB) dominated the microbial communities of raw milk cheese, while Gram-negative microorganisms of animal or soil origin dominated the microbiota of raw milk and cheese-processing environments. Although functional screening of the metagenomic library did not recover potential quorum-sensing inhibitors, in silico analysis using an in-house database built specifically for this study identified homologues to several genes encoding proteins with predicted quorum-quenching activity, among which, the QsdH hydrolase was the most abundant. In silico screening of the library identified LAB, and especially Lactococcus lactis, as a relevant reservoir of AR determinants in cheese. Functional screening of the library allowed the isolation of 13 recombinant clones showing an increased resistance toward ampicillin, which in all cases was accompanied by a reduced susceptibility to a wide range of β-lactam antibiotics. This study shows that the dairy-processing environment is a rich reservoir of AR determinants, which vary by sample source, and suggests that combining next-generation sequencing with functional metagenomics can be of use in overcoming the limitations of both approaches. IMPORTANCE The study shows the potential of functional metagenomics analyses to uncover the diversity of functions in microbial communities prevailing in dairy products and their processing environments, evidencing that lactic acid bacteria (LAB) dominate the cheese microbiota, whereas Gram-negative microorganisms of animal or soil origin dominate the microbiota of milk and cheese-processing environments. The functional and in silico screening of the library allowed the identification of LAB, and especially Lactococcus lactis, as a relevant reservoir of antimicrobial resistance (AR) determinants in cheese. Quorum-quenching (QQ) determinants were not recovered through the execution of wet-lab function-based screenings but were detected through in silico sequencing-based analysesSIThis work was supported by funding from the Science Foundation Ireland (SFI) (grant number 13/SIRG/2157), Fundación BBVA, and the Spanish Ministry of Science, Innovation and Universities (grant number AGL2016-78085-P). C.J.W. and P.D.C. are supported by Science Foundation Ireland (SFI) (grant numbers 12/RC/2273 and 16/SP/ 3827)American Society for MicrobiologyTecnologia de los AlimentosFacultad de Veterinaria2020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://journals.asm.org/doi/10.1128/msystems.00723-19https://hdl.handle.net/10612/21012reponame:BULERIA. Repositorio Institucional de la Universidad de Leóninstname:Universidad de LeónIngléshttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:buleria.unileon.es:10612/210122026-06-24T12:43:27Z
dc.title.none.fl_str_mv Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
title Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
spellingShingle Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
Alexa, Elena-Alexandra
Tecnología de los alimentos
Antibiotic resistance
Food safety
Functional metagenomics
Dairy products
Quorum quenching
3309 Tecnología de Los Alimentos
title_short Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
title_full Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
title_fullStr Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
title_full_unstemmed Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
title_sort Dairy Products and Dairy-Processing Environments as a Reservoir of Antibiotic Resistance and Quorum-Quenching Determinants as Revealed through Functional Metagenomics
dc.creator.none.fl_str_mv Alexa, Elena-Alexandra
Walsh, Calum J.
Coughlan, Laura M.
Awad, Amal
Simon, Cezara A.
Ruiz, Lorena
Crispie, Fiona
Cotter, Paul D.
Álvarez Ordóñez, Avelino
author Alexa, Elena-Alexandra
author_facet Alexa, Elena-Alexandra
Walsh, Calum J.
Coughlan, Laura M.
Awad, Amal
Simon, Cezara A.
Ruiz, Lorena
Crispie, Fiona
Cotter, Paul D.
Álvarez Ordóñez, Avelino
author_role author
author2 Walsh, Calum J.
Coughlan, Laura M.
Awad, Amal
Simon, Cezara A.
Ruiz, Lorena
Crispie, Fiona
Cotter, Paul D.
Álvarez Ordóñez, Avelino
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Tecnologia de los Alimentos
Facultad de Veterinaria
dc.subject.none.fl_str_mv Tecnología de los alimentos
Antibiotic resistance
Food safety
Functional metagenomics
Dairy products
Quorum quenching
3309 Tecnología de Los Alimentos
topic Tecnología de los alimentos
Antibiotic resistance
Food safety
Functional metagenomics
Dairy products
Quorum quenching
3309 Tecnología de Los Alimentos
description [EN] Here, the role of the dairy-processing chain as a reservoir of antimicrobial resistance (AR) determinants and a source of novel biocontrol quorum-sensing inhibitors is assessed through a functional metagenomics approach. A metagenomic library comprising ~22,000 recombinant clones was built from DNA isolated from raw milk, raw milk cheeses, and cheese-processing environment swab samples. The high-throughput sequencing of 9,216 recombinant clones showed that lactic acid bacteria (LAB) dominated the microbial communities of raw milk cheese, while Gram-negative microorganisms of animal or soil origin dominated the microbiota of raw milk and cheese-processing environments. Although functional screening of the metagenomic library did not recover potential quorum-sensing inhibitors, in silico analysis using an in-house database built specifically for this study identified homologues to several genes encoding proteins with predicted quorum-quenching activity, among which, the QsdH hydrolase was the most abundant. In silico screening of the library identified LAB, and especially Lactococcus lactis, as a relevant reservoir of AR determinants in cheese. Functional screening of the library allowed the isolation of 13 recombinant clones showing an increased resistance toward ampicillin, which in all cases was accompanied by a reduced susceptibility to a wide range of β-lactam antibiotics. This study shows that the dairy-processing environment is a rich reservoir of AR determinants, which vary by sample source, and suggests that combining next-generation sequencing with functional metagenomics can be of use in overcoming the limitations of both approaches. IMPORTANCE The study shows the potential of functional metagenomics analyses to uncover the diversity of functions in microbial communities prevailing in dairy products and their processing environments, evidencing that lactic acid bacteria (LAB) dominate the cheese microbiota, whereas Gram-negative microorganisms of animal or soil origin dominate the microbiota of milk and cheese-processing environments. The functional and in silico screening of the library allowed the identification of LAB, and especially Lactococcus lactis, as a relevant reservoir of antimicrobial resistance (AR) determinants in cheese. Quorum-quenching (QQ) determinants were not recovered through the execution of wet-lab function-based screenings but were detected through in silico sequencing-based analyses
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://journals.asm.org/doi/10.1128/msystems.00723-19
https://hdl.handle.net/10612/21012
url https://journals.asm.org/doi/10.1128/msystems.00723-19
https://hdl.handle.net/10612/21012
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:BULERIA. Repositorio Institucional de la Universidad de León
instname:Universidad de León
instname_str Universidad de León
reponame_str BULERIA. Repositorio Institucional de la Universidad de León
collection BULERIA. Repositorio Institucional de la Universidad de León
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,301629

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