Genomic Analysis of Carbapenem-Resistant Pseudomonas aeruginosa Isolated From Urban Rivers Confirms Spread of Clone Sequence Type 277 Carrying Broad Resistome and Virulome Beyond the Hospital.

Fernanda Esposito,Brenda Cardoso,Bruna Fuga,Quézia Moura,Herrison Fontana,Danny Fuentes-Castillo,Adriana Cardenas-Arias,Nilton Lincopan

doi:10.3389/fmicb.2021.701921

Abstract

The dissemination of antibiotic-resistant priority pathogens beyond hospital settings is both a public health and an environmental problem. In this regard, high-risk clones exhibiting a multidrug-resistant (MDR) or extensively drug-resistant (XDR) phenotype have shown rapid adaptation at the human-animal-environment interface. In this study, we report genomic data and the virulence potential of the carbapenemase, São Paulo metallo-β-lactamase (SPM-1)-producing Pseudomonas aeruginosa strains (Pa19 and Pa151) isolated from polluted urban rivers, in Brazil. Bioinformatic analysis revealed a wide resistome to clinically relevant antibiotics (carbapenems, aminoglycosides, fosfomycin, sulfonamides, phenicols, and fluoroquinolones), biocides (quaternary ammonium compounds) and heavy metals (copper), whereas the presence of exotoxin A, alginate, quorum sensing, types II, III, and IV secretion systems, colicin, and pyocin encoding virulence genes was associated with a highly virulent behavior in the Galleria mellonella infection model. These results confirm the spread of healthcare-associated critical-priority P. aeruginosa belonging to the MDR sequence type 277 (ST277) clone beyond the hospital, highlighting that the presence of these pathogens in environmental water samples can have clinical implications for humans and other animals.

Highlights

Carbapenem-resistant Pseudomonas aeruginosa are a leading cause of hospital-acquired infections and have become a health priority (Tacconelli et al, 2018)
Two carbapenemase (SPM-1)-producing P. aeruginosa sequence type 277 (ST277) (Pa19 and Pa151 strains) isolated from impacted urban rivers in São Paulo, Brazil, were sequenced. As this clone has been endemic in Brazilian hospitals, being identified in migratory birds (Figure 1), we have performed a comparative analysis with publically available genomes obtained from ST277 lineages from human infections
Previous studies have reported the occurrence of carbapenemase (KPC-2)-producing Klebsiella pneumoniae belonging to the clonal group CG258 and OXA-23-positive A. baumannii ST79 in the Tietê River (Oliveira et al, 2014; Turano et al, 2016), supporting an anthropogenic trend, most likely due to hospital wastewater discharge and domestic wastewaters effluents (Nascimento et al, 2017; Bartley et al, 2019; Böger et al, 2021; Popa et al, 2021)

Summary

Introduction

Carbapenem-resistant Pseudomonas aeruginosa are a leading cause of hospital-acquired infections and have become a health priority (Tacconelli et al, 2018). Along with MDR P. aeruginosa, the critical pathogens WHO list included Acinetobacter baumannii and bacteria from Enterobacterales group (Tacconelli et al, 2018). They were categorized as critical priority through the use of multi-criteria, including being resistant to a large number of antibiotics, such as carbapenems and third generation cephalosporins, the best available options for treating MDR pathogens (Babu et al, 2020). Based on WHO list priority pathogens criteria, which included pathogen mortality, hospital and environment transmissibility and limited treatment options, recognition and genomic characterization of critical priority pathogens is an essential first step to understanding their dynamic of acquisition/dissemination and to development of preventive intervention strategies (Hendriksen et al, 2019). We report genomic data and the virulence potential of carbapenem-resistant SPM-1-positive P. aeruginosa strains isolated from polluted urban rivers, in Brazil

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