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Characterization of a novel multi-resistant Pseudomonas juntendi strain from China with chromosomal blaVIM−2 and a megaplasmid coharboring blaIMP−1−like and blaOXA−1

BMC Genomics volume 25, Article number: 774 (2024) Cite this article

Abstract

Background

Pseudomonas juntendi is a newly identified opportunistic pathogen, of which we have limited understanding. P. juntendi strains are often multidrug resistant, which complicates clinical management of infection.

Methods

A strain of Pseudomonas juntendi (strain L4326) isolated from feces was characterized by MALDI-TOF-MS and Average Nucleotide Identity BLAST. This strain was further subject to whole-genome sequencing and Maximum Likelihood phylogenetic analysis. The strain was phenotypically characterized by antimicrobial susceptibility testing and conjugation assays.

Results

We have isolated the novel P. juntendi strain L4236, which was multidrug resistant, but retained sensitivity to amikacin. L4236 harbored a megaplasmid that encoded blaOXA−1 and a novel blaIMP−1 resistance gene variant. P. juntendi strain L4236 was phylogenetically related to P. juntendi strain SAMN30525517.

Conclusion

A rare P. juntendi strain was isolated from human feces in southern China with a megaplasmid coharboring blaIMP−1−like and blaOXA−1. Antimicrobial selection pressures may have driven acquisition of drug-resistance gene mutations and carriage of the megaplasmid.

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Background

In recent years, novel members of the genus Pseudomonas have been described due to the development of identification techniques [1]. The Pseudomonas putida group (P. putida G) consists of over 21 environmental species, which are largely sensitive to antibiotics [2]. However, in recent years, P. putida G strains harboring resistance genes have been detected. Pseudomonas juntendi is an understudied member of the putida group. In Brazil, a carbapenem-resistant P. juntendi clinical isolate harboring blaBKC−1 was recently reported [3]. Similarly, a carbapenem-resistant P. juntendi urine isolate encoding blaIMP−1 was identified in China [4]. A P. juntendi strain isolated from a farm in China was found to encode tmexCD3-toprJ3 [5], and a metallo-β-lactamase (MBLs) producing strain isolated from Poland was found to belong to the MBL-producing P. putida (MPPP) group [6].

MBLs are well known determinants of carbapenem resistance, and consist of NDM, VIM, IMP, AIM, SPM, DIM, KPC, and OXA variants [7]. VIM and IMP belong to Class B, while OXA belongs to Class D, in accordance with the classification proposed by Ambler [8]. Acquisition of carbapenemase genes are not random with respect to strain phylogeny [9]. Most IMP variants can be expressed in conjunction with other drug-resistance genes, and more than 29 IMP variants have been identified in clinically important Gram-negative bacilli [10]. ​First detected in Japan in 1994 [11], IMP-1 shares a comparable capacity as NDM-1 for hydrolyzing meropenem [12]. VIM-2 is a soluble MBL [13], which was identified in a strain isolated from a Portuguese patient in 1995 [14]. Members of P. putida G have been suggested to be a reservoir of blaVIM−2 genes [15]. Furthermore, OXA, first identified in the 1960s [16], promotes resistance to aminopenicillins and ureidopenicillin, and displays high-level capacity to hydrolyze oxacillin, methicillin, and cloxacillin [17]. Antibiotic resistance genes can integrate into plasmids which are then acquired by clinical pathogens, leading to difficulties in clinical management, and a substantial burden on world health [18].

Our study has identified a novel Pseudomonas juntendi strain, L4326, which co-harbors blaIMP−1−like, blaOXA−1 genes on a large plasmid, and blaVIM−2 gene on a chromosome. We also identified a novel variant of IMP-1 (IMP-1-like), and provide mechanistic insights into the development of drug resistance in this emerging pathogen.

Materials and methods

Strain identification and antimicrobial susceptibility testing (AST)

A strain was isolated from the feces of a patient at a teaching hospital in the Zhejiang province, China. The isolate was characterized as Pseudomonas juntendi by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF/MS) (Bruker Daltonik, Bremen, Germany) [19], and Basic Local Alignment Search Tool (BLAST) analysis, and was designated strain L4326.

Subsequently, AST [20] was performed by broth microdilution for polymyxin B, or agar dilution for other drugs, according to the criteria of the Clinical and Laboratory Standards Institute (CLSI) and the European Committee on Antimicrobial Susceptibility Testing (EUCAST). Escherichia coli ATCC25922 and Pseudomonas aeruginosa ATCC27853 were used as control strains. P. juntendi L4326 plated on Mueller-Hinton (MH) agar medium was incubated at 37℃ for 20 h, and the minimum inhibitory concentrations were taken as the first concentration to inhibit growth.

Bacterial whole-genome sequencing and downstream analysis

Total DNA from P. juntendi L4326 was extracted using the QIAamp DNA Microbiome kit (QIAamp, Germany) according to the manufacturer’s instructions. Genome sequencing was performed using the Illumina NovaSeq 6000 (Illumina, San Diego, CA, United States), and Oxford Nanopore sequencing (Oxford Nanopore Technologies, Oxford, UK) platforms. The whole genome was assembled with Unicycler v0.4.7, and coding sequences were annotated using Prokka v1.14.5. Acquired antimicrobial resistance (AMR) genes were identified using ResFinder 4.1 (https://cge.cbs.dtu.dk/services/ResFinder/), and virulence genes were identified using the Virulence factor database (VFDB) (http://www.mgc.ac.cn/). PlasmidFinder (https://cge.cbs.dtu.dk/services/PlasmidFinder/) was used to characterize plasmid types present in the genome sequence. The genetic context of blaIMP−1−like, blaOXA−1, and blaVIM−2 were visualized with Easyfig 2.3 (http://mjsull.github.io/Easyfig/files.html). Analysis of the plasmid from P. juntendi L4326 was performed by BLAST Ring Image Generator (BRIG) (http://sourceforge.net/projects/brig/). Maximum likelihood phylogenetic analysis of gene and protein sequences was performed using MEGAX (version 10.1.7), following ClustalW alignment of sequences, and the resulting tree was visualized using the Interactive Tree of Life (iTOL, https://itol.embl.de).

The average nucleotide identity based on BLAST (ANIb)

Analysis of P. juntendi L4326 taxonomy by ANIb was performed using pyani stools (v. 0.2.3) [21]. Whole-genome alignments were generated by nucleotide BLAST (BLASTN) [22]. After pairwise alignment, the percent nucleotide identity of all genomes was subject to hierarchical clustering by a Euclidean distance metric. A heatmap was generated including P. juntendi L4326 and nine reference strains, where the color scale bar indicates ANI percentages from 75% (blue) to 100% (red), and 95 % identity was considered the threshold of a species boundary.

Maximum likelihood phylogenetic analysis

Phylogenetic analysis was performed using a General Time Reversible model and the Maximum Likelihood method. The evolutionary relationship between each taxon was discerned from a consensus tree derived from 1000 bootstrap replicates. MEGA11 [23] was used to generate an initial tree using BioNJ and Neighbor-Joining algorithms from a matrix of pairwise distances. The tree topology was refined using the superior log likelihood value through the Maximum Composite Likelihood approach [24]. Model evolutionary rate differences between sites (5 categories; +G, parameter = 0.0500) were estimated by discrete Gamma distribution.

Conjugation experiments

E. coli J53 was used as a recipient strain for conjugation experiments as previously described [25]. Briefly, 200 mg/L sodium azide (NaN3) and 2 mg/L meropenem were dissolved in MH broth (OXOID, Hampshire, UK). The broth was subsequently inoculated with P. juntendi L4326 and the recipient strain, before culturing until the logarithmic growth phase. Plasmid conjugation was determined using a PCR-based method.

Results

Isolation and identification of Pseudomonas juntendi L4326

Fresh fecal samples were plated on MacConkey Agar Medium supplemented with meropenem. Multiple resulting colonies were present after 18 h growth at 37 °C. MALDI-TOF/MS analysis revealed that one of these strains belonged to the genus Pseudomonas. ANIb analysis (Fig. 1) subsequently revealed high degrees of similarity between this isolate and P. juntendi PP 2463 SAMN24966705. Conversely, the ANIb percentage identity of our isolate with other strains within the Pseudomonas genus was low. We therefore named this strain Pseudomonas juntendi L4326.

Fig. 1
figure 1

A heatmap displaying ANIb scores between P. juntendi L4326 and eight reference strains of the genus Pseudomonas. ANIb percentage identities below 0.7 are gray, while a gradient of blue to red indicates values from 0.7 to 1

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AST of this strain indicated a multidrug-resistant phenotype (Table 1), with detected resistance to piperacillin/tazobactam, ceftazidime, cefepime, imipenem, meropenem, ceftazidime/avibactam, aztreonam, polymyxin B, gentamicin, levofloxacin, and ciprofloxacin. This strain was however sensitive to amikacin.

Table 1 AST results of Pseudomonas Juntendi L4326
Full size table

Genomics features of P. juntendi L4326 and comparison to other P. juntendi strains

P. juntendi L4326 consists of a 5,403,450 bp chromosome and a 501,858 bp large plasmid, with a total GC content of 61.7%. Interestingly, we detected no similarity of this large plasmid to other plasmids in public databases (Fig. 2). Both a novel 250 kbp-length drug resistance gene named blaIMP−1−like and a known drug resistance gene named blaOXA−1 were located on this giant plasmid. As expected, horizontal transfer of the large plasmid was undetected using our conjugation assay.

Fig. 2
figure 2

Map of the megaplasmid from P. juntendi L4326 coharboring blaIMP−1−like and blaOXA−1 genes. The two inner circles indicate the GC content and skew, while the outer circle represents key genes. Red represents hypothetical proteins, green represents mobile elements, and blue represents AMR and other genes

Full size image

Comparison of L4326 to 40 previously described P. juntendi strains worldwide, revealed high degrees of similarity to P. juntendi strain SAMN30525517, which was isolated in America and may represent a source of transmission (Fig. 3).

Fig. 3
figure 3

Maximum-likelihood phylogenetic tree of P. juntendi L4326 and 40 other P. juntendi isolates. The tree was discerned from an alignment generated using Roary. Branches are colored based on bootstrap support values from red (0.62) to green [1] using the Maximum Composite Likelihood approach. Sample type, collection date, isolation source, and geographic location are indicated

Full size image

Genetic context of the IMP-1-like gene

To further verify the novel IMP allele detected in strain L4326, we analyzed both the genomic sequence and protein structure of IMP 1-100 (http://bldb.eu/BLDB.php?prot=B1#IMP). The protein structure of L4326-IMP was the same as IMP-1 (Fig. 4A). By comparing the SNP differences, we found that the protein SNPs of IMP-1-like and IMP-1 are identical, but its gene sequence is closest to IMP-79 and IMP-98, with 3 SNP differences. The gene sequence revealed that L4326-IMP was a novel antibiotic resistance gene with high degrees of gene homology to IMP-79 and IMP-98 (Fig. 4B). Together, this indicates that we have identified a new mutant gene named IMP-1-like encoded on a novel megaplasmid.

Fig. 4
figure 4

Phylogenetic tree of IMP protein (A) and gene (B) sequences visualized using Interactive Tree of Life. The protein and gene sequences of IMP 1-100 and L4326-IMP were subject to BLAST analysis, and different colors indicate branch regions of interest. The location and origin of L4326-IMP are shown

Full size image

The genetic context of IMP-1-like and VIM-2 was predicted through comparison of related IMP-1 (Fig. 5A) and VIM-2 (Fig. 5B) genes in the NCBI database. IMP-1-like (L4326-IMP) shared sequence similarity with Pseudomonas sp. NY11382 plasmid pNY11382-IMP (CP097104), Pseudomonas putida strain NY5709 plasmid pNY5709-IMP (MN961670), and Pseudomonas putida strain ZXPA-20 plasmid pZXPA-20-602k (CP061724). Among these, we considered that the genetic organization of “TnAs1-xerC-blaIMP−1−like-aacA4-blaOXA−1-ant1-emrE” may have arisen from “TnAs1-xerC-blaIMP−34-emrE” through insertion of the antibiotic resistance gene “blaOXA−1” via an integrating mobile element exploiting the xerC site and Xer (IMEX) recombination [26]. EmrE belongs to the Small Multidrug Resistance (SMR) transporter family, which may promote further drug resistance [27]. In addition, VIM-2 (L4326-VIM) had a comparable genetic context to that of Pseudomonas putida strain NY5709 plasmid pNY5709-IMP (MN961670), Pseudomonas fulva strain ZDHY316 plasmid pVIM-24-ZDHY316 (CP064945), and Pseudomonas sp. NY11382 plasmid pNY11382-IMP (CP097104).

Fig. 5
figure 5

The genetic context of blaIMP−1−like (A) and blaVIM−2 (B) compared with three similar plasmids. Red arrows indicate blaIMP−1 and blaVIM−2, while blue arrows indicate insertion sequences (IS) and transposons (Tn). Gray shading represents a high degree of homology among these plasmids

Full size image

Discussion

​We have isolated and characterized a novel strain of Pseudomonas juntendi carrying a giant plasmid coharboring blaIMP−1−like and blaOXA−1 and a chromosomal copy of blaVIM−2. In addition to the first isolation of a P. juntendi strain from a clinical sample in southern China, we also identified IMP-1-like, a novel resistance gene.

The genus Pseudomonas are not typically considered constituents of the healthy gut microbiome [28], and are associated with intestinal infection and intestinal barrier dysfunction [29]. 79% of Pseudomonas strains from humans in a previous study from Ethiopia were MDR [30]. Within the genus, P. juntendi are not a commonly isolated species in the clinic. Tohya M et al. [31]. first identified and officially named P. juntendi in 2019. The first clinical isolate of P. juntendi was isolated in northern China in 2022 [4]. We have subsequently identified P. juntendi strain L4326 in southern China carrying a large plasmid encoding the blaIMP−1−like gene. There are currently 40 described strains of P. juntendi worldwide, seven of which were isolated in China. P. juntendi L4236, however, shows high degrees of sequence similarity with P. juntendi SAMN30525517, which was isolated in America, indicating that our strain may have been introduced to China through migration. The P. juntendi L4326 plasmid is larger than previously described plasmids, and notably encoded multiple antibiotic resistances genes including blaIMP−1−like and blaOXA−1. The World Health Organization (WHO) has indicated that critically important pathogens such as those of the genus Pseudomonas are often isolated from clinical infections and display resistance to last-resort antibiotics including colistin [32]. Drug resistance is an enormous burden on public health and government financial expenditure [33]. While P. juntendi L4326 showed resistance to multiple antibiotics, this strain remained susceptible to amikacin.

P. juntendi is considered a potential hazard due to expression of blaIMP and blaVIM which promote carbapenem resistance [4]. Since its earliest detection in a strain of Pseudomonas aeruginosa in Japan [34], up to 100 IMP-1 variants have been described. Expression of the IMP-1 metallo-β-lactamase is a major determinant of decreased antibiotic sensitivity [35]. Compared with IMP 1-100, IMP-1-like protein of P. juntendi L4326 is the same as IMP-1 protein, while IMP-1-like gene of P. juntendi L4326 is similar as IMP-1 gene, which manifested the fact that IMP-1-like might be shifted from IMP-1. Drug-resistance genes are prone to the accumulation of mutations under antibiotic selection pressure. The continuing emergence of novel drug-resistance genes is a further reminder that we should consider the rational use of antibiotics.

P. juntendi L4326 encodes not only IMP-1-like, but also VIM-2. The existence of blaVIM−2 in P. juntendi L4326 indicate that P. putida G complex serves as a reservoir for blaVIM−2 which may spread to other clinically relevant pathogens [15].

Together, our findings clearly highlight that both the rapid spread of P. juntendi in China, and the emergence of antibiotic resistance gene mutations under selection pressure warrant careful monitoring.

Conclusion

We isolated a strain of P. juntendi encoding a novel IMP-1-like gene from a patient in southern China. This strain contains both a 501,858 bp megaplasmid coharboring blaIMP−1−like and blaOXA−1, and a chromosomal copy of blaVIM−2. These findings indicate the rapid transmission of P. juntendi in China, and highlight the need to monitor emergence of novel drug-resistance mutations.

Data availability

Sequencing data of Pseudomonas juntendi L4326 are available from the NCBI database under sample accession number SAMN37524096.

Abbreviations

AMR:

Acquired antimicrobial resistance

ANIb:

Average Nucleotide Identity based on BLAST

AST:

Antimicrobial susceptibility testing

BLAST:

Basic Local Alignment Search Tool

BRIG:

BLAST Ring Image Generator

CLSI:

Clinical and Laboratory Standards Institute

EUCAST:

European Committee on Antimicrobial Susceptibility Testing

IMEX:

Integrating mobile element exploiting Xer

MALDI-TOF-MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

MBLs:

Metallo-β-lactamases

MCL:

Maximum Composite Likelihood

MDR:

Multi-drug resistance

MH:

Mueller-Hinton

MICs:

Minimum inhibitory concentrations

MPPP:

MBL-producing P. putida

NaN3 :

Sodium azide

SMR:

Small Multidrug Resistance

VFDB:

Virulence factor database

WHO:

World Health Organization

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Acknowledgements

We are grateful to the reviewers who helped to improve this paper.

Funding

This work was supported by the Fundamental Research Funds for the Central Universities, grant No. 2022ZFJH003.

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Author notes

  1. Shiman Jiang and Yaling Li have contributed equally to this work and share first authorship.

Authors and Affiliations

  1. State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, National Medical Center for Infectious Diseases, Zhejiang University School of Medicine, 79 Qingchun Rd, Hangzhou City, 310003, China

    Shiman Jiang, Kefan Bi, Sisi Yang, He Xia, Shengjie Li, Hui Chen & Lanjuan Li

  2. Department Health Management Center, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China

    Yaling Li

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  1. Shiman Jiang
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Contributions

SMJ and YLL did conceptualization, methodology, experiment execution, and writing; KFB prepared statistical analysis, reviewing and editing; SSY, HX, SJL, and HC prapred editing; LJL is responsible for funding acquisition and supervision. All authors read and gave permission for the manuscript.

Corresponding author

Correspondence to Lanjuan Li.

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Ethical approval

All experimental protocols were approved by Ethics Committee of the First Affiliated Hospital, Zhejiang University School of Medicine (Issuing number: IIT20200594A). Informed consent was waived by Ethics Committee of the First Affiliated Hospital of Zhejiang University School of Medicine due to the study’s observational nature mainly focused on bacteria and did no interventions to patients, additionally, patient information was anonymized. All experiments were performed in compliance with the relevant laws and institutional guidelines in accordance with the ethical standards of the Declaration of Helsinki.

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The authors declare no competing interests.

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Jiang, S., Li, Y., Bi, K. et al. Characterization of a novel multi-resistant Pseudomonas juntendi strain from China with chromosomal blaVIM−2 and a megaplasmid coharboring blaIMP−1−like and blaOXA−1. BMC Genomics 25, 774 (2024). https://doi.org/10.1186/s12864-024-10688-2

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Keywords

BMC Genomics

ISSN: 1471-2164

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