Volume 25, Issue 12 p. 3035-3051
RESEARCH ARTICLE

Integrons, transposons and IS elements promote diversification of multidrug resistance plasmids and adaptation of their hosts to antibiotic pollutants from pharmaceutical companies

Masaki Shintani

Masaki Shintani

Department of Engineering, Graduate School of Integrated Science and Technology, Shizuoka University, Shizuoka, Japan

Research Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan

Japan Collection of Microorganisms, RIKEN BioResource Research Center, Ibaraki, Japan

Contribution: Formal analysis (equal), Funding acquisition (equal), ​Investigation (equal), Visualization (equal), Writing - original draft (equal), Writing - review & editing (equal)

Search for more papers by this author
Gisle Vestergaard

Gisle Vestergaard

Chr. Hansen A/S, Hoersholm, Denmark

Contribution: Data curation (equal), Formal analysis (equal), ​Investigation (equal), Methodology (equal), Validation (equal), Writing - original draft (equal)

Search for more papers by this author
Milena Milaković

Milena Milaković

Division for Marine and Environmental Research, Ruđer Bošković Institute, Croatia

Contribution: Formal analysis (equal)

Search for more papers by this author
Susanne Kublik

Susanne Kublik

Research Unit for Comparative Microbiome Analysis, Helmholtz Zentrum München, Zagreb, Germany

Contribution: Data curation (equal)

Search for more papers by this author
Kornelia Smalla

Kornelia Smalla

Institute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Braunschweig, Germany

Contribution: Supervision (equal), Validation (equal), Writing - review & editing (equal)

Search for more papers by this author
Michael Schloter

Michael Schloter

Research Unit for Comparative Microbiome Analysis, Helmholtz Zentrum München, Zagreb, Germany

Contribution: Validation (equal), Writing - review & editing (equal)

Search for more papers by this author
Nikolina Udiković-Kolić

Corresponding Author

Nikolina Udiković-Kolić

Division for Marine and Environmental Research, Ruđer Bošković Institute, Croatia

Correspondence

Nikolina Udiković-Kolić, Division for Marine and Environmental Research, Ruđer Bošković Institute, Zagreb, Croatia.

Email: [email protected]

Contribution: Conceptualization (equal), Funding acquisition (equal), Project administration (lead), Supervision (lead), Validation (equal), Writing - original draft (equal), Writing - review & editing (equal)

Search for more papers by this author
First published: 01 September 2023
Citations: 1

Masaki Shintani and Gisle Vestergaard contributed equally to this study.

Abstract

Plasmids are important vehicles for the dissemination of antibiotic resistance genes (ARGs) among bacteria by conjugation. Here, we determined the complete nucleotide sequences of nine different plasmids previously obtained by exogenous plasmid isolation from river and creek sediments and wastewater from a pharmaceutical company. We identified six IncP/P-1ε plasmids and single members of IncL, IncN and IncFII-like plasmids. Genetic structures of the accessory regions of the IncP/P-1ε plasmids obtained implied that multiple insertions and deletions had occurred, mediated by different transposons and Class 1 integrons with various ARGs. Our study provides compelling evidence that Class 1 integrons, Tn402-like transposons, Tn3-like transposons and/or IS26 played important roles in the acquisition of ARGs across all investigated plasmids. Our plasmid sequencing data provide new insights into how these mobile genetic elements could mediate the acquisition and spread of ARGs in environmental bacteria.

Graphical Abstract

Plasmids are the carriers of antibiotic resistance genes (ARGs). We have deciphered the complete nucleotide sequences of nine unique plasmids in pharmaceutical wastewater and aquatic environments. These tiny molecular machines are cleverly equipped with integrons and transposons, enabling the acquisition and transfer of diverse ARGs. Our findings shed light on how these genetic elements facilitate the spread of resistance among bacteria in both environmental and public health settings, with significant implications for combating drug-resistant infections.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

DATA AVAILABILITY STATEMENT

The plasmid sequences and their CDS information were deposited in DDBJ/GenBank under accession numbers LC746219-LC746227. The other data that support the findings of this study are available from the corresponding author upon reasonable request.