Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions

Detalhes bibliográficos
Autor(a) principal: Pereira, AP
Data de Publicação: 2023
Outros Autores: Antunes, Patrícia, Bierge, P, Willems, RJL, Corander, J, Coque, TM, Pich, OQ, Peixe, L., Freitas, AR, Novais, Carla
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: https://hdl.handle.net/10216/156796
Resumo: Quaternary ammonium compounds (QACs) have been extensively used in the community, healthcare facilities, and food chain, in concentrations between 20 and 30,000 mg/L. Enterococcus faecalis and Enterococcus faecium are ubiquitous in these settings and are recognized as nosocomial pathogens worldwide, but QACs' activity against strains from diverse epidemiological and genomic backgrounds remained largely unexplored. We evaluated the role of Enterococcus isolates from different sources, years, and clonal lineages as hosts of QACs tolerance genes and their susceptibility to QACs in optimal, single-stress and cross-stress growth conditions. Only 1% of the Enterococcus isolates included in this study and 0.5% of publicly available Enterococcus genomes carried qacA/B, qacC, qacG, qacJ, qacZ, qrg, bcrABC or oqxAB genes, shared with >60 species of Bacillota,Pseudomonadota,Actinomycetota,or Spirochaetota. with >60 species of Bacillota, Pseudomonadota, Actinomycetota, or Spirochaetota. These genes were generally found within close proximity of antibiotics and/or metals resistance genes. The minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of benzalkonium chloride (BC) and didecyldimethylammonium chloride ranged between 0.5 and 4 mg/L(microdilution:37 degrees C/20h/pH = 7/aerobiosis)chloride ranged between 0.5 and 4 mg/L (microdilution: 37 degrees C/20 h/pH = 7/aerobiosis) for 210 E. faecalis and E. faecium isolates (two isolates carrying qacZ). Modified growth conditions (e.g., 22 degrees C/pH = 5) increased MICBC/MBCBC (maximum of eightfold and MBCBC =16mg/L)and changed bacterial growth kinetics under BC toward later stationary = 16 mg/L) and changed bacterial growth kinetics under BC toward later stationary phases in both species, including in isolates without QACs tolerance genes. In conclusion, Enterococcus are susceptible to in-use QACs concentrations and rarely carry QACs tolerance genes. However, their potential gene exchange with different microbiota, the decreased susceptibility to QACs under specific environmental conditions, and the presence of subinhibitory QACs concentrations in various settings may contribute to the selection of particular strains and, thus, require a One Health strategy to maintain QACs effectiveness.
id RCAP_09f4ff2c777bec19968a77f4670ca11d
oai_identifier_str oai:repositorio-aberto.up.pt:10216/156796
network_acronym_str RCAP
network_name_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository_id_str 7160
spelling Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditionsCiências da Saúde, Ciências médicas e da saúdeHealth sciences, Medical and Health sciencesQuaternary ammonium compounds (QACs) have been extensively used in the community, healthcare facilities, and food chain, in concentrations between 20 and 30,000 mg/L. Enterococcus faecalis and Enterococcus faecium are ubiquitous in these settings and are recognized as nosocomial pathogens worldwide, but QACs' activity against strains from diverse epidemiological and genomic backgrounds remained largely unexplored. We evaluated the role of Enterococcus isolates from different sources, years, and clonal lineages as hosts of QACs tolerance genes and their susceptibility to QACs in optimal, single-stress and cross-stress growth conditions. Only 1% of the Enterococcus isolates included in this study and 0.5% of publicly available Enterococcus genomes carried qacA/B, qacC, qacG, qacJ, qacZ, qrg, bcrABC or oqxAB genes, shared with >60 species of Bacillota,Pseudomonadota,Actinomycetota,or Spirochaetota. with >60 species of Bacillota, Pseudomonadota, Actinomycetota, or Spirochaetota. These genes were generally found within close proximity of antibiotics and/or metals resistance genes. The minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of benzalkonium chloride (BC) and didecyldimethylammonium chloride ranged between 0.5 and 4 mg/L(microdilution:37 degrees C/20h/pH = 7/aerobiosis)chloride ranged between 0.5 and 4 mg/L (microdilution: 37 degrees C/20 h/pH = 7/aerobiosis) for 210 E. faecalis and E. faecium isolates (two isolates carrying qacZ). Modified growth conditions (e.g., 22 degrees C/pH = 5) increased MICBC/MBCBC (maximum of eightfold and MBCBC =16mg/L)and changed bacterial growth kinetics under BC toward later stationary = 16 mg/L) and changed bacterial growth kinetics under BC toward later stationary phases in both species, including in isolates without QACs tolerance genes. In conclusion, Enterococcus are susceptible to in-use QACs concentrations and rarely carry QACs tolerance genes. However, their potential gene exchange with different microbiota, the decreased susceptibility to QACs under specific environmental conditions, and the presence of subinhibitory QACs concentrations in various settings may contribute to the selection of particular strains and, thus, require a One Health strategy to maintain QACs effectiveness.20232023-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/10216/156796eng2165-049710.1128/spectrum.02324-23Pereira, APAntunes, PatríciaBierge, PWillems, RJLCorander, JCoque, TMPich, OQPeixe, L.Freitas, ARNovais, Carlainfo:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-01-26T04:54:20Zoai:repositorio-aberto.up.pt:10216/156796Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-20T01:57:33.165207Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
title Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
spellingShingle Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
Pereira, AP
Ciências da Saúde, Ciências médicas e da saúde
Health sciences, Medical and Health sciences
title_short Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
title_full Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
title_fullStr Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
title_full_unstemmed Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
title_sort Unraveling Enterococcus susceptibility to quaternary ammonium compounds: genes, phenotypes, and the impact of environmentalc onditions
author Pereira, AP
author_facet Pereira, AP
Antunes, Patrícia
Bierge, P
Willems, RJL
Corander, J
Coque, TM
Pich, OQ
Peixe, L.
Freitas, AR
Novais, Carla
author_role author
author2 Antunes, Patrícia
Bierge, P
Willems, RJL
Corander, J
Coque, TM
Pich, OQ
Peixe, L.
Freitas, AR
Novais, Carla
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Pereira, AP
Antunes, Patrícia
Bierge, P
Willems, RJL
Corander, J
Coque, TM
Pich, OQ
Peixe, L.
Freitas, AR
Novais, Carla
dc.subject.por.fl_str_mv Ciências da Saúde, Ciências médicas e da saúde
Health sciences, Medical and Health sciences
topic Ciências da Saúde, Ciências médicas e da saúde
Health sciences, Medical and Health sciences
description Quaternary ammonium compounds (QACs) have been extensively used in the community, healthcare facilities, and food chain, in concentrations between 20 and 30,000 mg/L. Enterococcus faecalis and Enterococcus faecium are ubiquitous in these settings and are recognized as nosocomial pathogens worldwide, but QACs' activity against strains from diverse epidemiological and genomic backgrounds remained largely unexplored. We evaluated the role of Enterococcus isolates from different sources, years, and clonal lineages as hosts of QACs tolerance genes and their susceptibility to QACs in optimal, single-stress and cross-stress growth conditions. Only 1% of the Enterococcus isolates included in this study and 0.5% of publicly available Enterococcus genomes carried qacA/B, qacC, qacG, qacJ, qacZ, qrg, bcrABC or oqxAB genes, shared with >60 species of Bacillota,Pseudomonadota,Actinomycetota,or Spirochaetota. with >60 species of Bacillota, Pseudomonadota, Actinomycetota, or Spirochaetota. These genes were generally found within close proximity of antibiotics and/or metals resistance genes. The minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of benzalkonium chloride (BC) and didecyldimethylammonium chloride ranged between 0.5 and 4 mg/L(microdilution:37 degrees C/20h/pH = 7/aerobiosis)chloride ranged between 0.5 and 4 mg/L (microdilution: 37 degrees C/20 h/pH = 7/aerobiosis) for 210 E. faecalis and E. faecium isolates (two isolates carrying qacZ). Modified growth conditions (e.g., 22 degrees C/pH = 5) increased MICBC/MBCBC (maximum of eightfold and MBCBC =16mg/L)and changed bacterial growth kinetics under BC toward later stationary = 16 mg/L) and changed bacterial growth kinetics under BC toward later stationary phases in both species, including in isolates without QACs tolerance genes. In conclusion, Enterococcus are susceptible to in-use QACs concentrations and rarely carry QACs tolerance genes. However, their potential gene exchange with different microbiota, the decreased susceptibility to QACs under specific environmental conditions, and the presence of subinhibitory QACs concentrations in various settings may contribute to the selection of particular strains and, thus, require a One Health strategy to maintain QACs effectiveness.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023-01-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv https://hdl.handle.net/10216/156796
url https://hdl.handle.net/10216/156796
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 2165-0497
10.1128/spectrum.02324-23
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
repository.mail.fl_str_mv
_version_ 1799137061963300865