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(Reference retrieved automatically from Web of Science through information on FAPESP grant and its corresponding number as mentioned in the publication by the authors.)

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

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Lopes, Ralf [1] ; Fuentes-Castillo, Danny [2, 3] ; Fontana, Herrison [4, 3] ; Rodrigues, Larissa [4, 3] ; Dantas, Karine [1] ; Cerdeira, Louise [5] ; Henriques, Isabel [6, 7] ; Lincopan, Nilton [1, 4, 3]
Total Authors: 8
[1] Univ Sao Paulo, Inst Biomed Sci, Dept Microbiol, Sao Paulo - Brazil
[2] Univ Sao Paulo, Sch Vet Med & Anim Sci, Dept Pathol, Sao Paulo - Brazil
[3] One Hlth Brazilian Resistance Project OneBR, Sao Paulo - Brazil
[4] Univ Sao Paulo, Sch Pharm, Dept Clin Anal, Sao Paulo - Brazil
[5] Monash Univ, Cent Clin Sch, Dept Infect Dis, Melbourne, Vic - Australia
[6] Univ Coimbra, Fac Sci & Technol, Dept Life Sci, Coimbra - Portugal
[7] Univ Aveiro, Ctr Environm & Marine Studies CESAM, Aveiro - Portugal
Total Affiliations: 7
Document type: Journal article
Source: MSYSTEMS; v. 6, n. 1 JAN-FEB 2021.
Web of Science Citations: 1

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 beta-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 Enrerobacrerales 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 beta-lactamases (ESBL)-producing Enterobacrerales 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 beta-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 coil 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. (AU)

FAPESP's process: 16/08593-9 - Pan-Resistome of beta-lactamase (KPC-2, CTX-M-8, CTX-M-15)-producing Klebsiella pneumoniae and Escherichia coli isolates endemic in Brazil
Grantee:Nilton Erbet Lincopan Huenuman
Support Opportunities: Regular Research Grants
FAPESP's process: 15/21325-0 - Comparative analysis of the resistome of Klebsiella pneumoniae XDR (NDM-1/KPC-2) belonging to the endemic high-risk clonal complex CC258
Grantee:Louise Teixeira Cerdeira
Support Opportunities: Scholarships in Brazil - Doctorate