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. 2024 Jan 26;14(1):2246.
doi: 10.1038/s41598-024-51819-9.

Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh

Spencer Mark Mondol  1 , Israt Islam  1 , Md Rafiul Islam  1 , Shahriar Kabir Shakil  1   2 , Nadira Naznin Rakhi  1 , Jannatul Ferdous Mustary  3 , Amiruzzaman  4 , Donald James Gomes  1 , Hussain Md Shahjalal  5 , Md Mizanur Rahaman  6
Affiliations

Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh

Spencer Mark Mondol et al. Sci Rep. .

Abstract

The increasing antimicrobial resistance in Providencia stuartii (P. stuartii) worldwide, particularly concerning for immunocompromised and burn patients, has raised concern in Bangladesh, where the significance of this infectious opportunistic pathogen had been previously overlooked, prompting a need for investigation. The two strains of P. stuartii (P. stuartii SHNIBPS63 and P. stuartii SHNIBPS71) isolated from wound swab of two critically injured burn patients were found to be multidrug-resistant and P. stuartii SHNIBPS63 showed resistance to all the 22 antibiotics tested as well as revealed the co-existence of blaVEB-6 (Class A), blaNDM-1 (Class B), blaOXA-10 (Class D) beta lactamase genes. Complete resistance to carbapenems through the production of NDM-1, is indicative of an alarming situation as carbapenems are considered to be the last line antibiotic to combat this pathogen. Both isolates displayed strong biofilm-forming abilities and exhibited resistance to copper, zinc, and iron, in addition to carrying multiple genes associated with metal resistance and the formation of biofilms. The study also encompassed a pangenome analysis utilizing a dataset of eighty-six publicly available P. stuartii genomes (n = 86), revealing evidence of an open or expanding pangenome for P. stuartii. Also, an extensive genome-wide analysis of all the P. stuartii genomes revealed a concerning global prevalence of diverse antimicrobial resistance genes, with a particular alarm raised over the abundance of carbapenem resistance gene blaNDM-1. Additionally, this study highlighted the notable genetic diversity within P. stuartii, significant informations about phylogenomic relationships and ancestry, as well as potential for cross-species transmission, raising important implications for public health and microbial adaptation across different environments.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Genome maps of the analyzed genomes. (A) P. stuartii SHNIBPS63, (B) P. stuartii SHNIBPS71.
Figure 2
Figure 2
Plasmid mapping and annotation showing antimicrobial resistance genes carried by the plasmids and genes associated with their dissemination. (A) Plasmid mapping of Providencia stuartii SHNIBPS63. (B) Plasmid mapping of Providencia stuartii SHNIBPS71.
Figure 3
Figure 3
Mapping of antimicrobial resistance genes and mobile genetic elements in carbapenem resistant Providencia stuartii SHNIBPS63. (A) Antimicrobial resistance genes mapping. (B) The organization of mobile genetic elements in the genome. (C) Organization and mapping of antimicrobial resistance genes with surrounding mobile genetic elements.
Figure 4
Figure 4
Presence of arn and sap operon in the genome of P. stuartii SHNIBPS63. (A) Genomic organization of the arnBCADTEF operon. (B) Genomic organization of the sapABCDF operon.
Figure 5
Figure 5
Antimicrobial resistance genes analysis of publicly available 86 genomes of P. stuartii. (A) Abundance of antimicrobial resistance genes based on categories. (B) Abundance of different type of beta lactamase genes in P. stuartii. (C) Abundance of different variants of beta lactamase genes in P. stuartii where the high occurrence of blaOXA-10, blaNDM-1 and blaTEM-1 is depicted with red bars.
Figure 6
Figure 6
Pangenome and comparative genome analysis. (A) Pangenome and pangenome based phylogenetic analysis of 86 different strains of P. stuartii worldwide including the two test isolates of this study. (B) Comparative scenario of the core and cloud/accessory genome in the pangenome of P. stuartii. (C) Comparative analysis of each part of the pangenome showing respective number of genes.
Figure 7
Figure 7
(A) SNP-based phylogenomic analysis of all the 86 genomes of P. stuartii worldwide including the two test isolates of this study. (B) Comparative genomic feature analysis of the representative 21 isolates of P. stuartii from different countries and sources including the two test isolates of this study. (C) Genome alignment of the genomes using Mauve depicting the variability in the genomes of P. stuartii.
Figure 8
Figure 8
Genome wide pathogenicity analysis of the representative 21 isolates of P. stuartii from different countries and sources including the two test isolates of this study. (A) Pathogenicity profiling of the isolates based on whole genome sequence analysis. (B) Whole proteome comparison of pathogenic and non-pathogenic P. stuartii isolated from different sources.
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