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Diversification and prevalence of the quinolone resistance crpP genes and the crpP-carrying Tn6786-related integrative and conjugative elements in Pseudomonas aeruginosa.

ABSTRACT: The quinolone resistance crpP genes can mediate decreased susceptibility to quinolones. However, diversification and prevalence of crpP genes and crpP-carrying integrative and conjugative elements (ICEs) still need to be elucidated. In this study, genome sequencing was conducted for 200 Chinese Pseudomonas aeruginosa isolates, 16 of which were fully sequenced. All the 37 available CrpP variants were collected for phylogenetic analysis, 10 CrpP enzymes were chosen to conduct cloning and antimicrobial susceptibility test, and 22 crpP-carrying Tn6786-related ICEs were selected for detail genetic dissection analysis. Then, typing/nomenclature schemes for crpP variants and crpP-carrying ICEs were established for the first time. The 10 representative CrpP enzymes were confirmed to mediate decreased susceptibility to one to three quinolones. Tn6786-related ICEs displayed high-level diversification in both nucleotide sequences and modular structures. Mainly, massive gene acquisition/loss occurred across the whole genomes of Tn6786-related ICEs. 53.5% (107/200) of the tested clinical P. aeruginosa isolates from China carried crpP genes, which were exclusively located within chromosome-borne Tn6786-related ICEs. The crpP-carrying ICEs were at active stages of evolution and had the high potential to be an important vector for the dissemination of resistance genes besides crpP. The present study furthered the understanding of the bioinformatics and epidemiology of crpP genes and crpP-carrying ICEs.

SUBMITTER: Zhu Z

PROVIDER: S-EPMC8381794 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Integrative conjugative elements (ICE) are a diverse group of chromosomally integrated, self-transmissible mobile genetic elements (MGE) that are active in shaping the functions of bacteria and bacterial communities. Each type of ICE carries a characteristic set of core genes encoding functions essential for maintenance and self-transmission, and cargo genes that endow on hosts phenotypes beneficial for niche adaptation. An important area to which ICE can contribute beneficial functions is the biodegradation of xenobiotic compounds. In the biodegradation realm, the best-characterized ICE is ICEclc, which carries cargo genes encoding for ortho-cleavage of chlorocatechols (clc genes) and aminophenol metabolism (amn genes). The element was originally identified in the 3-chlorobenzoate-degrader Pseudomonas knackmussii B13, and the closest relative is a nearly identical element in Burkholderia xenovorans LB400 (designated ICEclc-B13 and ICEclc-LB400, respectively). In the present report, genome sequencing of the o-chlorobenzoate degrader Pseudomonas aeruginosa JB2 was used to identify a new member of the ICEclc family, ICEclc-JB2. The cargo of ICEclc-JB2 differs from that of ICEclc-B13 and ICEclc-LB400 in consisting of a unique combination of genes that encode for the utilization of o-halobenzoates and o-hydroxybenzoate as growth substrates (ohb genes and hyb genes, respectively) and which are duplicated in a tandem repeat. Also, ICEclc-JB2 lacks an operon of regulatory genes (tciR-marR-mfsR) that is present in the other two ICEclc, and which controls excision from the host. Thus, the mechanisms regulating intracellular behavior of ICEclc-JB2 may differ from that of its close relatives. The entire tandem repeat in ICEclc-JB2 can excise independently from the element in a process apparently involving transposases/insertion sequence associated with the repeats. Excision of the repeats removes important niche adaptation genes from ICEclc-JB2, rendering it less beneficial to the host. However, the reduced version of ICEclc-JB2 could now acquire new genes that might be beneficial to a future host and, consequently, to the survival of ICEclc-JB2. Collectively, the present identification and characterization of ICEclc-JB2 provides insights into roles of MGE in bacterial niche adaptation and the evolution of catabolic pathways for biodegradation of xenobiotic compounds.

Project description:BACKGROUND:Pseudomonas aeruginosa is a cause of nosocomial infections, especially in patients with cystic fibrosis and burn wounds. PAO1 strain and its derivatives are widely used to study the biology of this bacterium, however recent studies demonstrated differences in the genomes and phenotypes of derivatives from different laboratories. RESULTS:Here we report the genome sequence of P. aeruginosa PAO1161 laboratory strain, a leu-, RifR, restriction-modification defective PAO1 derivative, described as the host of IncP-8 plasmid FP2, conferring the resistance to mercury. Comparison of PAO1161 genome with PAO1-UW sequence revealed lack of an inversion of a large genome segment between rRNA operons and 100 nucleotide polymorphisms, short insertions and deletions. These included a change in leuA, resulting in E108K substitution, which caused leucine auxotrophy and a mutation in rpoB, likely responsible for the rifampicin resistance. Nonsense mutations were detected in PA2735 and PA1939 encoding a DNA methyltransferase and a putative OLD family endonuclease, respectively. Analysis of revertants in these two genes showed that PA2735 is a component of a restriction-modification system, independent of PA1939. Moreover, a 12 kb RPG42 prophage and a novel 108 kb PAPI-1 like integrative conjugative element (ICE) encompassing a mercury resistance operon were identified. The ICEPae1161 was transferred to Pseudomonas putida cells, where it integrated in the genome and conferred the mercury resistance. CONCLUSIONS:The high-quality P. aeruginosa PAO1161 genome sequence provides a reference for further research including e.g. investigation of horizontal gene transfer or comparative genomics. The strain was found to carry ICEPae1161, a functional PAPI-1 family integrative conjugative element, containing loci conferring mercury resistance, in the past attributed to the FP2 plasmid of IncP-8 incompatibility group. This indicates that the only known member of IncP-8 is in fact an ICE.

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Diversification and prevalence of the quinolone resistance crpP genes and the crpP-carrying Tn6786-related integrative and conjugative elements in Pseudomonas aeruginosa.

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