Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?

ABSTRACT 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...

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Autores principales:	Ralf Lopes, Danny Fuentes-Castillo, Herrison Fontana, Larissa Rodrigues, Karine Dantas, Louise Cerdeira, Isabel Henriques, Nilton Lincopan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/129e72da9ebf465da0c6658c99b516cf
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spelling	oai:doaj.org-article:129e72da9ebf465da0c6658c99b516cf2021-12-02T17:07:26ZEndophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?10.1128/mSystems.01125-202379-5077https://doaj.org/article/129e72da9ebf465da0c6658c99b516cf2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01125-20https://doaj.org/toc/2379-5077ABSTRACT 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 blaCTX-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.Ralf LopesDanny Fuentes-CastilloHerrison FontanaLarissa RodriguesKarine DantasLouise CerdeiraIsabel HenriquesNilton LincopanAmerican Society for MicrobiologyarticleE. coli ST648E. coli ST38K. pneumoniae CC307CTX-M-15foodOne HealthMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health Microbiology QR1-502
spellingShingle	E. coli ST648 E. coli ST38 K. pneumoniae CC307 CTX-M-15 food One Health Microbiology QR1-502 Ralf Lopes Danny Fuentes-Castillo Herrison Fontana Larissa Rodrigues Karine Dantas Louise Cerdeira Isabel Henriques Nilton Lincopan Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?
description	ABSTRACT 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 blaCTX-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.
format	article
author	Ralf Lopes Danny Fuentes-Castillo Herrison Fontana Larissa Rodrigues Karine Dantas Louise Cerdeira Isabel Henriques Nilton Lincopan
author_facet	Ralf Lopes Danny Fuentes-Castillo Herrison Fontana Larissa Rodrigues Karine Dantas Louise Cerdeira Isabel Henriques Nilton Lincopan
author_sort	Ralf Lopes
title	Endophytic Lifestyle of Global Clones of Extended-Spectrum β-Lactamase-Producing Priority Pathogens in Fresh Vegetables: a Trojan Horse Strategy Favoring Human Colonization?
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?
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/129e72da9ebf465da0c6658c99b516cf
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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?

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