Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?
Autor(a) principal: | |
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Data de Publicação: | 2021 |
Outros Autores: | , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/10316/105277 https://doi.org/10.1128/mSystems.01125-20 |
Resumo: | The global spread of antibiotic-resistant bacteria and their resistance genes is a critical issue that is no longer restricted to hospital settings, but also represents a growing problem involving environmental and food safety. In this study, we have performed a microbiological and genomic investigation of critical priority pathogens resistant to broad-spectrum cephalosporins and showing endophytic lifestyles in fresh vegetables sold in a country with high endemicity of extended-spectrum β-lactamases (ESBLs). We report the isolation of international high-risk clones of CTX-M-15-producing Escherichia coli, belonging to clonal complexes CC38 and CC648, and Klebsiella pneumoniae of complex CC307 from macerated tissue of surface-sterilized leaves of spinach, cabbage, arugula, and lettuce. Regardless of species, all ESBL-positive isolates were able to endophytically colonize common bean (Phaseolus vulgaris) seedlings, showed resistance to acid pH, and had a multidrug-resistant (MDR) profile to clinically relevant antibiotics (i.e., broad-spectrum cephalosporins, aminoglycosides, and fluoroquinolones). Genomic analysis of CTX-M-producing endophytic Enterobacterales revealed a wide resistome (antibiotics, biocides, disinfectants, and pesticides) and virulome, and genes for endophytic fitness and for withstanding acidic conditions. Transferable IncFIB and IncHI2A plasmids carried bla CTX-M-15 genes and, additionally, an IncFIB plasmid (named pKP301cro) also harbored genes encoding resistance to heavy metals. These data support the hypothesis that fresh vegetables marketed for consumption can act as a figurative Trojan horse for the hidden spread of international clones of critical WHO priority pathogens producing ESBLs, and/or their resistance genes, to humans and other animals, which is a critical issue within a food safety and broader public and environmental health perspective.IMPORTANCE Extended-spectrum β-lactamases (ESBL)-producing Enterobacterales are a leading cause of human and animal infections, being classified as critical priority pathogens by the World Health Organization. Epidemiological studies have shown that spread of ESBL-producing bacteria is not a problem restricted to hospitals, but also represents a growing problem involving environmental and food safety. In this regard, CTX-M-type β-lactamases have become the most widely distributed and clinically relevant ESBLs worldwide. Here, we have investigated the occurrence and genomic features of ESBL-producing Enterobacterales in surface-sterilized fresh vegetables. We have uncovered that international high-risk clones of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae harboring a wide resistome and virulome, carry additional genes for endophytic fitness and resistance to acidic conditions. Furthermore, we have demonstrated that these CTX-M-15-positive isolates are able to endophytically colonize plant tissues. Therefore, we believe that fresh vegetables can act as a figurative Trojan horse for the hidden spread of critical priority pathogens exhibiting endophytic lifestyles. |
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Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?E. coli ST648E. coli ST38K. pneumoniae CC307CTX-M-15foodOne HealthESBLThe global spread of antibiotic-resistant bacteria and their resistance genes is a critical issue that is no longer restricted to hospital settings, but also represents a growing problem involving environmental and food safety. In this study, we have performed a microbiological and genomic investigation of critical priority pathogens resistant to broad-spectrum cephalosporins and showing endophytic lifestyles in fresh vegetables sold in a country with high endemicity of extended-spectrum β-lactamases (ESBLs). We report the isolation of international high-risk clones of CTX-M-15-producing Escherichia coli, belonging to clonal complexes CC38 and CC648, and Klebsiella pneumoniae of complex CC307 from macerated tissue of surface-sterilized leaves of spinach, cabbage, arugula, and lettuce. Regardless of species, all ESBL-positive isolates were able to endophytically colonize common bean (Phaseolus vulgaris) seedlings, showed resistance to acid pH, and had a multidrug-resistant (MDR) profile to clinically relevant antibiotics (i.e., broad-spectrum cephalosporins, aminoglycosides, and fluoroquinolones). Genomic analysis of CTX-M-producing endophytic Enterobacterales revealed a wide resistome (antibiotics, biocides, disinfectants, and pesticides) and virulome, and genes for endophytic fitness and for withstanding acidic conditions. Transferable IncFIB and IncHI2A plasmids carried bla CTX-M-15 genes and, additionally, an IncFIB plasmid (named pKP301cro) also harbored genes encoding resistance to heavy metals. These data support the hypothesis that fresh vegetables marketed for consumption can act as a figurative Trojan horse for the hidden spread of international clones of critical WHO priority pathogens producing ESBLs, and/or their resistance genes, to humans and other animals, which is a critical issue within a food safety and broader public and environmental health perspective.IMPORTANCE Extended-spectrum β-lactamases (ESBL)-producing Enterobacterales are a leading cause of human and animal infections, being classified as critical priority pathogens by the World Health Organization. Epidemiological studies have shown that spread of ESBL-producing bacteria is not a problem restricted to hospitals, but also represents a growing problem involving environmental and food safety. In this regard, CTX-M-type β-lactamases have become the most widely distributed and clinically relevant ESBLs worldwide. Here, we have investigated the occurrence and genomic features of ESBL-producing Enterobacterales in surface-sterilized fresh vegetables. We have uncovered that international high-risk clones of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae harboring a wide resistome and virulome, carry additional genes for endophytic fitness and resistance to acidic conditions. Furthermore, we have demonstrated that these CTX-M-15-positive isolates are able to endophytically colonize plant tissues. Therefore, we believe that fresh vegetables can act as a figurative Trojan horse for the hidden spread of critical priority pathogens exhibiting endophytic lifestyles.American Society for Microbiology2021-02-09info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://hdl.handle.net/10316/105277http://hdl.handle.net/10316/105277https://doi.org/10.1128/mSystems.01125-20eng2379-5077Lopes, RalfFuentes-Castillo, DannyFontana, HerrisonRodrigues, LarissaDantas, KarineCerdeira, LouiseHenriques, IsabelLincopan, Niltoninfo: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:RCAAP2023-02-14T11:14:32ZPortal AgregadorONG |
dc.title.none.fl_str_mv |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
title |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
spellingShingle |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? Lopes, Ralf E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health ESBL |
title_short |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
title_full |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
title_fullStr |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
title_full_unstemmed |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
title_sort |
Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization? |
author |
Lopes, Ralf |
author_facet |
Lopes, Ralf Fuentes-Castillo, Danny Fontana, Herrison Rodrigues, Larissa Dantas, Karine Cerdeira, Louise Henriques, Isabel Lincopan, Nilton |
author_role |
author |
author2 |
Fuentes-Castillo, Danny Fontana, Herrison Rodrigues, Larissa Dantas, Karine Cerdeira, Louise Henriques, Isabel Lincopan, Nilton |
author2_role |
author author author author author author author |
dc.contributor.author.fl_str_mv |
Lopes, Ralf Fuentes-Castillo, Danny Fontana, Herrison Rodrigues, Larissa Dantas, Karine Cerdeira, Louise Henriques, Isabel Lincopan, Nilton |
dc.subject.por.fl_str_mv |
E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health ESBL |
topic |
E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health ESBL |
description |
The global spread of antibiotic-resistant bacteria and their resistance genes is a critical issue that is no longer restricted to hospital settings, but also represents a growing problem involving environmental and food safety. In this study, we have performed a microbiological and genomic investigation of critical priority pathogens resistant to broad-spectrum cephalosporins and showing endophytic lifestyles in fresh vegetables sold in a country with high endemicity of extended-spectrum β-lactamases (ESBLs). We report the isolation of international high-risk clones of CTX-M-15-producing Escherichia coli, belonging to clonal complexes CC38 and CC648, and Klebsiella pneumoniae of complex CC307 from macerated tissue of surface-sterilized leaves of spinach, cabbage, arugula, and lettuce. Regardless of species, all ESBL-positive isolates were able to endophytically colonize common bean (Phaseolus vulgaris) seedlings, showed resistance to acid pH, and had a multidrug-resistant (MDR) profile to clinically relevant antibiotics (i.e., broad-spectrum cephalosporins, aminoglycosides, and fluoroquinolones). Genomic analysis of CTX-M-producing endophytic Enterobacterales revealed a wide resistome (antibiotics, biocides, disinfectants, and pesticides) and virulome, and genes for endophytic fitness and for withstanding acidic conditions. Transferable IncFIB and IncHI2A plasmids carried bla CTX-M-15 genes and, additionally, an IncFIB plasmid (named pKP301cro) also harbored genes encoding resistance to heavy metals. These data support the hypothesis that fresh vegetables marketed for consumption can act as a figurative Trojan horse for the hidden spread of international clones of critical WHO priority pathogens producing ESBLs, and/or their resistance genes, to humans and other animals, which is a critical issue within a food safety and broader public and environmental health perspective.IMPORTANCE Extended-spectrum β-lactamases (ESBL)-producing Enterobacterales are a leading cause of human and animal infections, being classified as critical priority pathogens by the World Health Organization. Epidemiological studies have shown that spread of ESBL-producing bacteria is not a problem restricted to hospitals, but also represents a growing problem involving environmental and food safety. In this regard, CTX-M-type β-lactamases have become the most widely distributed and clinically relevant ESBLs worldwide. Here, we have investigated the occurrence and genomic features of ESBL-producing Enterobacterales in surface-sterilized fresh vegetables. We have uncovered that international high-risk clones of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae harboring a wide resistome and virulome, carry additional genes for endophytic fitness and resistance to acidic conditions. Furthermore, we have demonstrated that these CTX-M-15-positive isolates are able to endophytically colonize plant tissues. Therefore, we believe that fresh vegetables can act as a figurative Trojan horse for the hidden spread of critical priority pathogens exhibiting endophytic lifestyles. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021-02-09 |
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 |
http://hdl.handle.net/10316/105277 http://hdl.handle.net/10316/105277 https://doi.org/10.1128/mSystems.01125-20 |
url |
http://hdl.handle.net/10316/105277 https://doi.org/10.1128/mSystems.01125-20 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
2379-5077 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
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 |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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