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

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, prompt...

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Main Authors: Spencer Mark Mondol, Israt Islam, Md. Rafiul Islam, Shahriar Kabir Shakil, Nadira Naznin Rakhi, Jannatul Ferdous Mustary, Amiruzzaman, Donald James Gomes, Hussain Md. Shahjalal, Md. Mizanur Rahaman
Format: Article
Language:English
Published: Nature Portfolio 2024-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-51819-9
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author Spencer Mark Mondol
Israt Islam
Md. Rafiul Islam
Shahriar Kabir Shakil
Nadira Naznin Rakhi
Jannatul Ferdous Mustary
Amiruzzaman
Donald James Gomes
Hussain Md. Shahjalal
Md. Mizanur Rahaman
author_facet Spencer Mark Mondol
Israt Islam
Md. Rafiul Islam
Shahriar Kabir Shakil
Nadira Naznin Rakhi
Jannatul Ferdous Mustary
Amiruzzaman
Donald James Gomes
Hussain Md. Shahjalal
Md. Mizanur Rahaman
author_sort Spencer Mark Mondol
collection DOAJ
description 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 bla VEB-6 (Class A), bla NDM-1 (Class B), bla OXA-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 bla NDM-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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spelling doaj.art-92a4d975bf4743c197fcf031e8f424972024-03-05T16:26:58ZengNature PortfolioScientific Reports2045-23222024-01-0114111510.1038/s41598-024-51819-9Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in BangladeshSpencer Mark Mondol0Israt Islam1Md. Rafiul Islam2Shahriar Kabir Shakil3Nadira Naznin Rakhi4Jannatul Ferdous Mustary5Amiruzzaman6Donald James Gomes7Hussain Md. Shahjalal8Md. Mizanur Rahaman9Department of Microbiology, University of DhakaDepartment of Microbiology, University of DhakaDepartment of Microbiology, University of DhakaDepartment of Microbiology, University of DhakaDepartment of Microbiology, University of DhakaMicrobiology Department, Sheikh Hasina National Institute of Burn and Plastic SurgeryDepartment of Medicine, Sir Salimullah Medical CollegeDepartment of Microbiology, University of DhakaDepartment of Biochemistry and Molecular Biology, Jahangirnagar UniversityDepartment of Microbiology, University of DhakaAbstract 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 bla VEB-6 (Class A), bla NDM-1 (Class B), bla OXA-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 bla NDM-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.https://doi.org/10.1038/s41598-024-51819-9
spellingShingle Spencer Mark Mondol
Israt Islam
Md. Rafiul Islam
Shahriar Kabir Shakil
Nadira Naznin Rakhi
Jannatul Ferdous Mustary
Amiruzzaman
Donald James Gomes
Hussain Md. Shahjalal
Md. Mizanur Rahaman
Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
Scientific Reports
title Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
title_full Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
title_fullStr Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
title_full_unstemmed Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
title_short Genomic landscape of NDM-1 producing multidrug-resistant Providencia stuartii causing burn wound infections in Bangladesh
title_sort genomic landscape of ndm 1 producing multidrug resistant providencia stuartii causing burn wound infections in bangladesh
url https://doi.org/10.1038/s41598-024-51819-9
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