In-depth resistome analysis by targeted metagenomics

BACKGROUND: Antimicrobial resistance is a major global health challenge. Metagenomics allows analyzing the presence and dynamics of "resistomes" (the ensemble of genes encoding antimicrobial resistance in a given microbiome) in disparate microbial ecosystems. However, the low sensitivity a...

Descripción completa

Detalles Bibliográficos
Autores: Lanza, Val F., Baquero, Fernando, Martínez, José Luís, Ramos-Ruíz, Ricardo, González-Zorn, Bruno, Andremont, Antoine, Sánchez-Valenzuela, Antonio, Ehrlich, Stanislav Dusko, Kennedy, Sean, Ruppé, Etienne, Schaik, Willem van, Willems, Rob J., Cruz, Fernando de la|||0000-0003-4758-6857, Coque, Teresa M.
Tipo de recurso: artículo
Fecha de publicación:2018
País:España
Institución:Universidad de Cantabria (UC)
Repositorio:UCrea Repositorio Abierto de la Universidad de Cantabria
Idioma:inglés
OAI Identifier:oai:repositorio.unican.es:10902/15932
Acceso en línea:http://hdl.handle.net/10902/15932
Access Level:acceso abierto
Palabra clave:Antimicrobial Resistance
Resistome
Metagenomics
Differential Abundance Analysis
Targeted Metagenomics
id ES_58e97e3d2fa478c4e349c1cac2a0517c
oai_identifier_str oai:repositorio.unican.es:10902/15932
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv In-depth resistome analysis by targeted metagenomics
title In-depth resistome analysis by targeted metagenomics
spellingShingle In-depth resistome analysis by targeted metagenomics
Lanza, Val F.
Antimicrobial Resistance
Resistome
Metagenomics
Differential Abundance Analysis
Targeted Metagenomics
title_short In-depth resistome analysis by targeted metagenomics
title_full In-depth resistome analysis by targeted metagenomics
title_fullStr In-depth resistome analysis by targeted metagenomics
title_full_unstemmed In-depth resistome analysis by targeted metagenomics
title_sort In-depth resistome analysis by targeted metagenomics
dc.creator.none.fl_str_mv Lanza, Val F.
Baquero, Fernando
Martínez, José Luís
Ramos-Ruíz, Ricardo
González-Zorn, Bruno
Andremont, Antoine
Sánchez-Valenzuela, Antonio
Ehrlich, Stanislav Dusko
Kennedy, Sean
Ruppé, Etienne
Schaik, Willem van
Willems, Rob J.
Cruz, Fernando de la|||0000-0003-4758-6857
Coque, Teresa M.
author Lanza, Val F.
author_facet Lanza, Val F.
Baquero, Fernando
Martínez, José Luís
Ramos-Ruíz, Ricardo
González-Zorn, Bruno
Andremont, Antoine
Sánchez-Valenzuela, Antonio
Ehrlich, Stanislav Dusko
Kennedy, Sean
Ruppé, Etienne
Schaik, Willem van
Willems, Rob J.
Cruz, Fernando de la|||0000-0003-4758-6857
Coque, Teresa M.
author_role author
author2 Baquero, Fernando
Martínez, José Luís
Ramos-Ruíz, Ricardo
González-Zorn, Bruno
Andremont, Antoine
Sánchez-Valenzuela, Antonio
Ehrlich, Stanislav Dusko
Kennedy, Sean
Ruppé, Etienne
Schaik, Willem van
Willems, Rob J.
Cruz, Fernando de la|||0000-0003-4758-6857
Coque, Teresa M.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidad de Cantabria
dc.subject.none.fl_str_mv Antimicrobial Resistance
Resistome
Metagenomics
Differential Abundance Analysis
Targeted Metagenomics
topic Antimicrobial Resistance
Resistome
Metagenomics
Differential Abundance Analysis
Targeted Metagenomics
description BACKGROUND: Antimicrobial resistance is a major global health challenge. Metagenomics allows analyzing the presence and dynamics of "resistomes" (the ensemble of genes encoding antimicrobial resistance in a given microbiome) in disparate microbial ecosystems. However, the low sensitivity and specificity of available metagenomic methods preclude the detection of minority populations (often present below their detection threshold) and/or the identification of allelic variants that differ in the resulting phenotype. Here, we describe a novel strategy that combines targeted metagenomics using last generation in-solution capture platforms, with novel bioinformatics tools to establish a standardized framework that allows both quantitative and qualitative analyses of resistomes. METHODS: We developed ResCap, a targeted sequence capture platform based on SeqCapEZ (NimbleGene) technology, which includes probes for 8667 canonical resistance genes (7963 antibiotic resistance genes and 704 genes conferring resistance to metals or biocides), and 2517 relaxase genes (plasmid markers) and 78,600 genes homologous to the previous identified targets (47,806 for antibiotics and 30,794 for biocides or metals). Its performance was compared with metagenomic shotgun sequencing (MSS) for 17 fecal samples (9 humans, 8 swine). ResCap significantly improves MSS to detect "gene abundance" (from 2.0 to 83.2%) and "gene diversity" (26 versus 14.9 genes unequivocally detected per sample per million of reads; the number of reads unequivocally mapped increasing up to 300-fold by using ResCap), which were calculated using novel bioinformatic tools. ResCap also facilitated the analysis of novel genes potentially involved in the resistance to antibiotics, metals, biocides, or any combination thereof. CONCLUSIONS: ResCap, the first targeted sequence capture, specifically developed to analyze resistomes, greatly enhances the sensitivity and specificity of available metagenomic methods and offers the possibility to analyze genes related to the selection and transfer of antimicrobial resistance (biocides, heavy metals, plasmids). The model opens the possibility to study other complex microbial systems in which minority populations play a relevant role.
publishDate 2018
dc.date.none.fl_str_mv 2018
2018-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
NA
http://purl.org/coar/version/c_be7fb7dd8ff6fe43
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10902/15932
url http://hdl.handle.net/10902/15932
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv European Commission http://dx.doi.org/10.13039/501100000780 Framework Programme Seven 612146
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BMC
publisher.none.fl_str_mv BMC
dc.source.none.fl_str_mv Microbiome. 2018 Jan 15;6(1):11
reponame:UCrea Repositorio Abierto de la Universidad de Cantabria
instname:Universidad de Cantabria (UC)
instname_str Universidad de Cantabria (UC)
reponame_str UCrea Repositorio Abierto de la Universidad de Cantabria
collection UCrea Repositorio Abierto de la Universidad de Cantabria
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869408576948142080
spelling In-depth resistome analysis by targeted metagenomicsLanza, Val F.Baquero, FernandoMartínez, José LuísRamos-Ruíz, RicardoGonzález-Zorn, BrunoAndremont, AntoineSánchez-Valenzuela, AntonioEhrlich, Stanislav DuskoKennedy, SeanRuppé, EtienneSchaik, Willem vanWillems, Rob J.Cruz, Fernando de la|||0000-0003-4758-6857Coque, Teresa M.Antimicrobial ResistanceResistomeMetagenomicsDifferential Abundance AnalysisTargeted MetagenomicsBACKGROUND: Antimicrobial resistance is a major global health challenge. Metagenomics allows analyzing the presence and dynamics of "resistomes" (the ensemble of genes encoding antimicrobial resistance in a given microbiome) in disparate microbial ecosystems. However, the low sensitivity and specificity of available metagenomic methods preclude the detection of minority populations (often present below their detection threshold) and/or the identification of allelic variants that differ in the resulting phenotype. Here, we describe a novel strategy that combines targeted metagenomics using last generation in-solution capture platforms, with novel bioinformatics tools to establish a standardized framework that allows both quantitative and qualitative analyses of resistomes. METHODS: We developed ResCap, a targeted sequence capture platform based on SeqCapEZ (NimbleGene) technology, which includes probes for 8667 canonical resistance genes (7963 antibiotic resistance genes and 704 genes conferring resistance to metals or biocides), and 2517 relaxase genes (plasmid markers) and 78,600 genes homologous to the previous identified targets (47,806 for antibiotics and 30,794 for biocides or metals). Its performance was compared with metagenomic shotgun sequencing (MSS) for 17 fecal samples (9 humans, 8 swine). ResCap significantly improves MSS to detect "gene abundance" (from 2.0 to 83.2%) and "gene diversity" (26 versus 14.9 genes unequivocally detected per sample per million of reads; the number of reads unequivocally mapped increasing up to 300-fold by using ResCap), which were calculated using novel bioinformatic tools. ResCap also facilitated the analysis of novel genes potentially involved in the resistance to antibiotics, metals, biocides, or any combination thereof. CONCLUSIONS: ResCap, the first targeted sequence capture, specifically developed to analyze resistomes, greatly enhances the sensitivity and specificity of available metagenomic methods and offers the possibility to analyze genes related to the selection and transfer of antimicrobial resistance (biocides, heavy metals, plasmids). The model opens the possibility to study other complex microbial systems in which minority populations play a relevant role.This study was supported by the European Commission, Seven Framework Program (EVOTARFP7-HEALTH-282004 for VFL, FB, JLM, AA, DE, ER, RJLW, WvS, FdlC, and TMC), the Joint Programming Initiative in Antimicrobial Resistance (JPIAMR Third call, STARCS, JPIAMR2016-AC16/00039 to TMC, RJLW, WvS), the Joint Programming Initiative in Water (JPI Water StARE JPIW2013-089-C02-01 to JLM) and the Ministry of Economy and Competitiveness of Spain (BIO2014-54507-R to JLM, and PLASWIRES-612146/FP7-ICT-2013-10 and BFU2014-55534-C2-1-P for FdlC). The authors also acknowledge the European Development Regional Fund “A way to achieve Europe” (ERDF) for co-founding the Spanish R&D National Plan 2012-2019 (BIO2014-54507-R to JLM, PI15-0512 to TMC, PI15-00818 to FB, and BFU2014-55534-C2-1-P to FdlC), CIBER (CIBER in Epidemiology and Public Health, CIBERESP; CB06/02/0053 to FB), the Spanish Network for Research on Infectious Diseases (REIPI RD12/0015 to JLM) and the Regional Government of Madrid (InGeMICSB2017/BMD-3691). Val F. Lanza was further funded by a Research Award Grant 2016 of the European Society for Clinical Microbiology and Infectious Diseases (ESCMID). Additional funding was from the Metagenopolis grant ANR-11-DPBS-0001 to DE.BMCUniversidad de Cantabria20182018-01-01journal articlehttp://purl.org/coar/resource_type/c_6501NAhttp://purl.org/coar/version/c_be7fb7dd8ff6fe43info:eu-repo/semantics/articlehttp://hdl.handle.net/10902/15932Microbiome. 2018 Jan 15;6(1):11reponame:UCrea Repositorio Abierto de la Universidad de Cantabriainstname:Universidad de Cantabria (UC)InglésengEuropean Commission http://dx.doi.org/10.13039/501100000780 Framework Programme Seven 612146open accesshttp://purl.org/coar/access_right/c_abf2Attribution 4.0 Internationalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositorio.unican.es:10902/159322026-06-02T12:39:31Z
score 15,300719