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. 2023 Mar 1:13:1130333.
doi: 10.3389/fcimb.2023.1130333. eCollection 2023.

Coexistence of tmexCD3-toprJ1b tigecycline resistance genes with two novel bla VIM-2-carrying and bla OXA-10-carrying transposons in a Pseudomononas asiatica plasmid

Qin Li  1 , Qiao Chen  1 , Shuang Liang  2 , Wei Wang  1 , Bingying Zhang  1 , Alberto J Martín-Rodríguez  3 , Qinghua Liang  1 , Feiyang Zhang  1 , Ling Guo  2 , Xia Xiong  4 , Renjing Hu  5 , Li Xiang  1 , Yingshun Zhou  1   6
Affiliations

Coexistence of tmexCD3-toprJ1b tigecycline resistance genes with two novel bla VIM-2-carrying and bla OXA-10-carrying transposons in a Pseudomononas asiatica plasmid

Qin Li et al. Front Cell Infect Microbiol. .

Abstract

Introduction: Tigecycline and carbapenems are considered the last line of defense against microbial infections. The co-occurrence of resistance genes conferring resistance to both tigecycline and carbapenems in Pseudomononas asiatica was not investigated.

Methods: P. asiatica A28 was isolated from hospital sewage. Antibiotic susceptibility testing showed resistance to carbapenem and tigecycline. WGS was performed to analyze the antimicrobial resistance genes and genetic characteristics. Plasmid transfer by conjugation was investigated. Plasmid fitness costs were evaluated in Pseudomonas aeruginosa transconjugants including a Galleria mellonella infection model.

Results: Meropenem and tigecycline resistant P. asiatica A28 carries a 199, 972 bp long plasmid PLA28.4 which harbors seven resistance genes. Sequence analysis showed that the 7113 bp transposon Tn7389 is made up of a class I integron without a 5'CS terminal and a complete tni module flanked by a pair of 25bp insertion repeats. Additionally, the Tn7493 transposon, 20.24 kp long, with a complete 38-bp Tn1403 IR and an incomplete 30-bp Tn1403 IR, is made up of partial skeleton of Tn1403, a class I integron harboring bla OXA-10, and a Tn5563a transposon. Moreover, one tnfxB3-tmexC3.2-tmexD3b-toprJ1b cluster was found in the plasmid and another one in the the chromosome. Furthermore, plasmid PLA28.4 could be conjugated to P. aeruginosa PAO1, with high fitness cost.

Discussion: A multidrug-resistant plasmid carrying tmexCD3-toprJ1b and two novel transposons carrying bla VIM-2 and bla OXA-10 -resistant genes was found in hospital sewage, increasing the risk of transmission of antibiotic-resistant genes. These finding highlight the necessary of controlling the development and spread of medication resistance requires continuous monitoring and management of resistant microorganisms in hospital sewage.

Keywords: Pseudomononas asiatica; blaVIM-2; hospital sewage; tigecycline resistance gene cluster; transposon.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Comparative structural analysis of PLA28.4 with other similar plasmids available in the NCBI nr database. Starting from the center: (1) GC content of PLA28.4 with an average of 56.36%. (2) GC skew, with a positive GC skew toward the inside and a negative GC skew toward the outside. (3) The reference plasmid PLA28.4 plasmid sequence (CP063457). (4) Plasmid pNK546b (MN583270). (5) Plasmid pCAR1.3 (AP013069). (6) Plasmid pCAR1 (AB088420). (7) Plasmid pCAR1.2 (AB474758). (8) Plasmid unnamed (CP034538). (8) Plasmid pZXPA-20-602k (CP061724). (9) Gene annotation. The Figure was constructed using BRIG.
Figure 2
Figure 2
Genetic environment of the novel Tn402-like transposon Tn7389 in P. asiatica A28. The construction of sequence comparison was performed using BLAST (http://blast.ncbi.nlm.nih.gov). Green arrows, integrases of a class of integrons; Light blue arrow: Tn402 tni module; red arrows, antibiotic resistance genes; purple arrows, Tn5563a-like genes; gray arrows, hypothetical protein.
Figure 3
Figure 3
Genetic environment of the novel Tn1403-like transposon Tn7493 in P. asiatica A28. The extents and directions of genes are shown by arrows labeled with gene names. The construction of sequence comparison was performed using BLAST (http://blast.ncbi.nlm.nih.gov).
Figure 4
Figure 4
The genetic context of the multidrug resistant efflux pump tnfxB3-tmexC3.2-tmexD3b-toprJ1b. The extents and directions of genes are shown by arrows labeled with gene names. Black arrows, tnfxB1-tmexCD1-toprJ1-like gene clusters; pink arrows, int and int-like genes, predicted to encode site-specific integrases; blue arrows, umuC and umuD; green arrows, mobile related genes; red arrows, antibiotic resistance genes; yellow arrows, mercury resistance genes; gray arrows, hypothetical protein. Regions of homology between 96% and 100% are shaded.
Figure 5
Figure 5
Fitness costs and stability of PLA28.4 in strain P. aeruginosa PAO1. (A) Growth curve of the transconjugant and recipient PAO1. (B) Biofilm formation of the transconjugant and recipient PAO1. (C, D) Survival of G. mellonella following infection with the transconjugant and recipient PAO1. *Statistically significant (p < 0.05), **statistically significant (p < 0.01), and ***statistically significant (p < 0.001).
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