Pathogenicity Genomic Island-Associated CrpP-Like Fluoroquinolone-Modifying Enzymes among Pseudomonas aeruginosa Clinical Isolates in Europe

Rosa, José Manuel Ortiz de la; Nordmann, Patrice; Poirel, Laurent

doi:10.1128/aac.00489-20

Cited by 15 publications

(24 citation statements)

References 15 publications

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“…As we were writing this manuscript, Ortiz de la Rosa et al used a PCR approach to screen the presence of the crpP gene among a collection of clonally unrelated and multidrug-resistant P. aeruginosa isolates recovered from hospitals in France and Switzerland [42]. The gene was present in around half the isolates screened, which is in agreement with our findings.…”

Section: Discussionsupporting

confidence: 87%

ICEs Are the Main Reservoirs of the Ciprofloxacin-Modifying crpP Gene in Pseudomonas aeruginosa

Botelho

Grosso

Peixe

2020

Genes

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The ciprofloxacin-modifying crpP gene was recently identified in a plasmid isolated from a Pseudomonas aeruginosa clinical isolate. Homologues of this gene were also identified in Escherichia coli, Klebsiella pneumoniae and Acinetobacter baumannii. We set out to explore the mobile elements involved in the acquisition and spread of this gene in publicly available and complete genomes of Pseudomonas spp. All Pseudomonas complete genomes were downloaded from NCBI’s Refseq library and were inspected for the presence of the crpP gene. The mobile elements carrying this gene were further characterized. The crpP gene was identified only in P. aeruginosa, in more than half of the complete chromosomes (61.9%, n = 133/215) belonging to 52 sequence types, of which the high-risk clone ST111 was the most frequent. We identified 136 crpP-harboring integrative and conjugative elements (ICEs), with 93.4% belonging to the mating-pair formation G (MPFG) family. The ICEs were integrated at the end of a tRNALys gene and were all flanked by highly conserved 45-bp direct repeats. The crpP-carrying ICEs contain 26 core genes (2.2% of all 1193 genes found in all the ICEs together), which are present in 99% or more of the crpP-harboring ICEs. The most frequently encoded traits on these ICEs include replication, transcription, intracellular trafficking and cell motility. Our work suggests that ICEs are the main vectors promoting the dissemination of the ciprofloxacin-modifying crpP gene in P. aeruginosa.

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Section: Discussionsupporting

confidence: 87%

ICEs Are the Main Reservoirs of the Ciprofloxacin-Modifying crpP Gene in Pseudomonas aeruginosa

Botelho

Grosso

Peixe

2020

Genes

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“…On the other hand, ten different crpP -encoding genes resulting in six CrpP enzymes were also found in 65.4% of MDR/XDR P. aeruginosa clinical isolates. Four of these CrpP variants (CrpP1, CrpP2, CrpP3 and CrpP4) have been previously found in P. aeruginosa isolates from other European countries [ 11 ], but two novel CrpP proteins (CrpP5 and CrpP6) were first identified in our study in two Portuguese centers.…”

Section: Discussionmentioning

confidence: 59%

“…According to recent literature, mutations in G7 and I26 position are non-commonly detected among the amino acid sequences of CrpP present in GenBank [6,26]. However, in both Portuguese and Spanish collections, CrpP variants carrying mutations in G7 were predominant, as recently described in other European countries [11]. It should be noted that the emergence and dissemination of modified CrpP variants in P. aeruginosa clinical isolates circulating in nosocomial settings such as ICUs could lead to the appearance and dissemination of novel crpP alleles with a higher ability to affect quinolones.…”

Section: Discussionmentioning

confidence: 68%

“…Interestingly, all crpP -encoding genes were located in PAGIs closely related to other genomic islands previously found in Europe between 2000 and 2015 [ 11 ]. Previous studies have demonstrated that xerD and parA genes contribute to transfer PAGI through P. aeruginosa strains, contributing to the dissemination of different antibiotic resistance mechanisms and virulence determinants and leading to the evolution and expansion of this species among different habitats [ 27 ].…”

Section: Discussionmentioning

confidence: 76%

“…Since then, ciprofloxacin-modifying crpP genes have been identified in P. aeruginosa as part of different mobile integrative and conjugative elements (ICEs) that frequently transfer horizontally [ 10 ]. However, homologous crpP genes have also been located in chromosomal pathogenicity genomic islands (PAGI) of P. aeruginosa clinical isolates recovered in France and Switzerland between 2000 and 2015 [ 11 ]. Additionally, a recent study has supported that mutations in the codons encoding Gly7, Asp9, Lys33 and Cys40 of CrpP protein generate modified CrpP variants that restore ciprofloxacin susceptibility [ 12 ].…”

Section: Introductionmentioning

confidence: 99%

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Presence of Chromosomal crpP-like Genes Is Not Always Associated with Ciprofloxacin Resistance in Pseudomonas aeruginosa Clinical Isolates Recovered in ICU Patients from Portugal and Spain

et al. 2021

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CrpP enzymes have been recently described as a novel ciprofloxacin-resistance mechanism. We investigated by whole genome sequencing the presence of crpP-genes and other mechanisms involved in quinolone resistance in MDR/XDR-Pseudomonas aeruginosa isolates (n = 55) with both ceftolozane-tazobactam susceptible or resistant profiles recovered from intensive care unit patients during the STEP (Portugal) and SUPERIOR (Spain) surveillance studies. Ciprofloxacin resistance was associated with mutations in the gyrA and parC genes. Additionally, plasmid-mediated genes (qnrS2 and aac(6′)-Ib-cr) were eventually detected. Ten chromosomal crpP-like genes contained in related pathogenicity genomic islands and 6 different CrpP (CrpP1-CrpP6) proteins were found in 65% (36/55) of the isolates. Dissemination of CrpP variants was observed among non-related clones of both countries, including the CC175 (Spain) high-risk clone and CC348 (Portugal) clone. Interestingly, 5 of 6 variants (CrpP1-CrpP5) carried missense mutations in an amino acid position (Gly7) previously defined as essential conferring ciprofloxacin resistance, and decreased ciprofloxacin susceptibility was only associated with the novel CrpP6 protein. In our collection, ciprofloxacin resistance was mainly due to chromosomal mutations in the gyrA and parC genes. However, crpP genes carrying mutations essential for protein function (G7, I26) and associated with a restored ciprofloxacin susceptibility were predominant. Despite the presence of crpP genes is not always associated with ciprofloxacin resistance, the risk of emergence of novel CrpP variants with a higher ability to affect quinolones is increasing. Furthermore, the spread of crpP genes in highly mobilizable genomic islands among related and non-related P. aeruginosa clones alert the dispersion of MDR pathogens in hospital settings.

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Antibiotic Resistance in Pseudomonas

Laborda

Hernando-Amado

Martínez

et al. 2022

Advances in Experimental Medicine and Biology

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Pathogenicity Genomic Island-Associated CrpP-Like Fluoroquinolone-Modifying Enzymes among Pseudomonas aeruginosa Clinical Isolates in Europe

Cited by 15 publications

References 15 publications

ICEs Are the Main Reservoirs of the Ciprofloxacin-Modifying crpP Gene in Pseudomonas aeruginosa

ICEs Are the Main Reservoirs of the Ciprofloxacin-Modifying crpP Gene in Pseudomonas aeruginosa

Presence of Chromosomal crpP-like Genes Is Not Always Associated with Ciprofloxacin Resistance in Pseudomonas aeruginosa Clinical Isolates Recovered in ICU Patients from Portugal and Spain

Antibiotic Resistance in Pseudomonas

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