Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome

Introduction: Streptococcus suis is a major pathogen for swine and human. Here we aimed to know the rates of antimicrobial resistance (AMR) in invasive S. suis isolates recovered along Spain between 2016 – 2021 and elucidate their genetic origin. Methods: Antibiotic susceptibility testing was perfor...

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Autores: Uruén, Cristina, Gimeno, Jorge, Sanz, Marina, Fraile Sauce, Lorenzo José, Marín, Clara M., Arenas, Jesús
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10459.1/465353
Acceso en línea:https://doi.org/10.3389/fcimb.2023.1329632
https://hdl.handle.net/10459.1/465353
Access Level:acceso abierto
Palabra clave:Streptococcus suis
Antimicrobial resistance (AMR)
Antimicrobial resistant genes
Mobile genetic elements
Streptococcus sp
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
title Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
spellingShingle Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
Uruén, Cristina
Streptococcus suis
Antimicrobial resistance (AMR)
Antimicrobial resistant genes
Mobile genetic elements
Streptococcus sp
title_short Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
title_full Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
title_fullStr Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
title_full_unstemmed Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
title_sort Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
dc.creator.none.fl_str_mv Uruén, Cristina
Gimeno, Jorge
Sanz, Marina
Fraile Sauce, Lorenzo José
Marín, Clara M.
Arenas, Jesús
author Uruén, Cristina
author_facet Uruén, Cristina
Gimeno, Jorge
Sanz, Marina
Fraile Sauce, Lorenzo José
Marín, Clara M.
Arenas, Jesús
author_role author
author2 Gimeno, Jorge
Sanz, Marina
Fraile Sauce, Lorenzo José
Marín, Clara M.
Arenas, Jesús
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Streptococcus suis
Antimicrobial resistance (AMR)
Antimicrobial resistant genes
Mobile genetic elements
Streptococcus sp
topic Streptococcus suis
Antimicrobial resistance (AMR)
Antimicrobial resistant genes
Mobile genetic elements
Streptococcus sp
description Introduction: Streptococcus suis is a major pathogen for swine and human. Here we aimed to know the rates of antimicrobial resistance (AMR) in invasive S. suis isolates recovered along Spain between 2016 – 2021 and elucidate their genetic origin. Methods: Antibiotic susceptibility testing was performed for 116 isolates of different genetic backgrounds and geographic origins against 18 antibiotics of 9 families. The association between AMR and genotypes and the origin of the isolates were statistically analyzed using Pearson´s chi-square test and the likelihood ratio. The antimicrobial resistant genes were identified by whole genome sequencing analysis and PCR screenings. Results: High AMR rates (>80%) were detected for tetracyclines, spectinomycin, lincosamides, and marbofloxacin, medium (20-40%) for sulphonamides/trimethoprim, tiamulin, penicillin G, and enrofloxacin, and low (< 20%) for florfenicol, and four additional β-lactams. The occurrence of multidrug resistance was observed in 90% of isolates. For certain antibiotics (penicillin G, enrofloxacin, marbofloxacin, tilmicosin, and erythromycin), AMR was significantly associated with particular sequence types (STs), geographic regions, age of pigs, and time course. Whole genome sequencing comparisons and PCR screenings identified 23 AMR genes, of which 19 were previously reported in S. suis (aph(3’)-IIIa, sat4, aadE, spw, aac(6’)-Ie-aph(2’’)-Ia, fexA, optrA, erm(B), mef(A/E), mrs(D), mph(C), lnu(B), lsa(E), vga(F), tet(M), tet(O), tet(O/W/32/O), tet(W)), and 4 were novel (aph(2’’)-IIIa, apmA, erm(47), tet(T)). These AMR genes explained the AMR to spectinomycin, macrolides, lincosamides, tiamulin, and tetracyclines. Several genes were located on mobile genetic elements which showed a variable organization and composition. As AMR gene homologs were identified in many human and animal pathogens, the resistome of S. suis has a different phylogenetic origin. Moreover, AMR to penicillin G, fluoroquinolones, and trimethoprim related to mutations in genes coding for target enzymes (pbp1a, pbp2b, pbp2x, mraY, gyrA, parC, and dhfr). Bioinformatic analysis estimated traits of recombination on target genes, also indicative of gene transfer events. Conclusions: Our work evidences that S. suis is a major contributor to AMR dissemination across veterinary and human pathogens. Therefore, control of AMR in S. suis should be considered from a One Health approach in regions with high pig production to properly tackle the issue of antimicrobial drug resistance.
publishDate 2024
dc.date.none.fl_str_mv 2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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status_str publishedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.3389/fcimb.2023.1329632
https://hdl.handle.net/10459.1/465353
url https://doi.org/10.3389/fcimb.2023.1329632
https://hdl.handle.net/10459.1/465353
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-114617RB-I00
Reproducció del document publicat a: https://doi.org/10.3389/fcimb.2023.1329632
Frontiers In Cellular And Infection Microbiology, 2023, vol. 13, 1329632, p. 1-18
dc.rights.none.fl_str_mv cc-by (c) Uruén et al., 2024
info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/4.0/
rights_invalid_str_mv cc-by (c) Uruén et al., 2024
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
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spelling Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistomeUruén, CristinaGimeno, JorgeSanz, MarinaFraile Sauce, Lorenzo JoséMarín, Clara M.Arenas, JesúsStreptococcus suisAntimicrobial resistance (AMR)Antimicrobial resistant genesMobile genetic elementsStreptococcus spIntroduction: Streptococcus suis is a major pathogen for swine and human. Here we aimed to know the rates of antimicrobial resistance (AMR) in invasive S. suis isolates recovered along Spain between 2016 – 2021 and elucidate their genetic origin. Methods: Antibiotic susceptibility testing was performed for 116 isolates of different genetic backgrounds and geographic origins against 18 antibiotics of 9 families. The association between AMR and genotypes and the origin of the isolates were statistically analyzed using Pearson´s chi-square test and the likelihood ratio. The antimicrobial resistant genes were identified by whole genome sequencing analysis and PCR screenings. Results: High AMR rates (>80%) were detected for tetracyclines, spectinomycin, lincosamides, and marbofloxacin, medium (20-40%) for sulphonamides/trimethoprim, tiamulin, penicillin G, and enrofloxacin, and low (< 20%) for florfenicol, and four additional β-lactams. The occurrence of multidrug resistance was observed in 90% of isolates. For certain antibiotics (penicillin G, enrofloxacin, marbofloxacin, tilmicosin, and erythromycin), AMR was significantly associated with particular sequence types (STs), geographic regions, age of pigs, and time course. Whole genome sequencing comparisons and PCR screenings identified 23 AMR genes, of which 19 were previously reported in S. suis (aph(3’)-IIIa, sat4, aadE, spw, aac(6’)-Ie-aph(2’’)-Ia, fexA, optrA, erm(B), mef(A/E), mrs(D), mph(C), lnu(B), lsa(E), vga(F), tet(M), tet(O), tet(O/W/32/O), tet(W)), and 4 were novel (aph(2’’)-IIIa, apmA, erm(47), tet(T)). These AMR genes explained the AMR to spectinomycin, macrolides, lincosamides, tiamulin, and tetracyclines. Several genes were located on mobile genetic elements which showed a variable organization and composition. As AMR gene homologs were identified in many human and animal pathogens, the resistome of S. suis has a different phylogenetic origin. Moreover, AMR to penicillin G, fluoroquinolones, and trimethoprim related to mutations in genes coding for target enzymes (pbp1a, pbp2b, pbp2x, mraY, gyrA, parC, and dhfr). Bioinformatic analysis estimated traits of recombination on target genes, also indicative of gene transfer events. Conclusions: Our work evidences that S. suis is a major contributor to AMR dissemination across veterinary and human pathogens. Therefore, control of AMR in S. suis should be considered from a One Health approach in regions with high pig production to properly tackle the issue of antimicrobial drug resistance.The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work received funding from Gobierno de Aragón (Department of I+D+I projects in priority lines, Grant agreement LMP58_21), and Ministerio de Ciencia e Innovación/Agencia Española de Investigación MCIN/AEI/10.13039/501100011033, as appropriate, by ERDF A way of making Europe by the European Union or by the European Union NextGenerationEU/PRTR (Gran agreement PID2020-114617RB-100). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Frontiers Media2024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://doi.org/10.3389/fcimb.2023.1329632https://hdl.handle.net/10459.1/465353reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)Inglésinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-114617RB-I00Reproducció del document publicat a: https://doi.org/10.3389/fcimb.2023.1329632Frontiers In Cellular And Infection Microbiology, 2023, vol. 13, 1329632, p. 1-18cc-by (c) Uruén et al., 2024info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/4.0/oai:recercat.cat:10459.1/4653532026-05-29T05:05:01Z
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