Colistin Resistance Mediated by Mcr-3-Related Phosphoethanolamine Transferase Genes in Aeromonas Species Isolated from Aquatic Environments in Avaga and Pakro Communities in the Eastern Region of Ghana

Samiratu Mahazu; Isaac Prah; Yusuke Ota; Takaya Hayashi; Masato Suzuki; Mitsunori Yoshida; Yoshihiko Hoshino; Yukihiro Akeda; Toshihiko Suzuki; Tomoko Ishino; Anthony Samuel Ablordey; Ryoichi Saito

doi:10.2147/IDR.S468000

Colistin Resistance Mediated by Mcr-3-Related Phosphoethanolamine Transferase Genes in Aeromonas Species Isolated from Aquatic Environments in Avaga and Pakro Communities in the Eastern Region of Ghana

Infect Drug Resist. 2024 Jul 15:17:3011-3023. doi: 10.2147/IDR.S468000. eCollection 2024.

Authors

Samiratu Mahazu^{1

2}, Isaac Prah^{1

3}, Yusuke Ota¹, Takaya Hayashi³, Masato Suzuki⁴, Mitsunori Yoshida⁵, Yoshihiko Hoshino⁵, Yukihiro Akeda⁶, Toshihiko Suzuki⁷, Tomoko Ishino², Anthony Samuel Ablordey⁸, Ryoichi Saito¹

Affiliations

¹ Department of Molecular Microbiology, Tokyo Medical and Dental University, Tokyo, Japan.
² Department of Parasitology and Tropical Medicine, Tokyo Medical and Dental University, Tokyo, Japan.
³ Department of Molecular Virology, Tokyo Medical and Dental University, Tokyo, Japan.
⁴ Antimicrobial Resistance Research Center, National Institute of Infectious Diseases, Tokyo, Japan.
⁵ Department of Mycobacteriology, Leprosy Research Center, National Institute of Infectious Diseases, Tokyo, Japan.
⁶ Department of Bacteriology I, National Institute of Infectious Diseases, Tokyo, Japan.
⁷ Department of Bacterial Pathogenesis, Tokyo Medical and Dental University, Tokyo, Japan.
⁸ Department of Bacteriology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, Ghana.

Abstract

Purpose: Colistin is classified by the World Health Organization (WHO) as a critically important and last-resort antibiotic for the treatment of infections caused by carbapenem-resistant bacteria. However, colistin resistance mediated by chromosomal mutations or plasmid-linked mobilized colistin resistance (mcr) genes has emerged.

Methods: Thirteen mcr-positive Aeromonas species isolated from water samples collected in Eastern Ghana were analyzed using whole-genome sequencing (WGS). Antimicrobial susceptibility was tested using the broth microdilution method. Resistome analysis was performed in silico using a web-based platform.

Results: The minimum inhibitory concentration (MIC) of colistin for all except three isolates was >4 µg/mL. Nine new sequence types were identified and whole-genome analysis revealed that the isolates harbored genes (mcr-3-related genes) that code for Lipid A phosphoethanolamine transferases on their chromosomes. BLAST analysis indicated that the amino acid sequences of the mcr-3-related genes detected varied from those previously reported and shared 79.04-99.86% nucleotide sequence identity with publicly available mcr-3 variants and mcr-3-related phosphoethanolamine transferases. Analysis of the genetic context of mcr-3-related genes revealed that the genetic environment surrounding mcr-3-related genes was diverse among the different species of Aeromonas but conserved among isolates of the same species. Mcr-3-related-gene-IS-mcr-3-related-gene segment was identified in three Aeromonas caviae strains.

Conclusion: The presence of mcr-3-related genes close to insertion elements is important for continuous monitoring to better understand how to control the mobilization and dissemination of antibiotic resistance genes.

Keywords: Aeromonas spp; colistin; mcr-3-related gene; phosphoethanolamine transferases; whole genome analysis.

Grants and funding

This research was supported by the Japan Agency for Medical Research and Development (AMED, URL: http://www.amed.go.jp/en/) under grant numbers JP20wm0125007 (TH, TS, TI, RS), JP20wm0225004 (MS, YH, TS, RS), JP20wm0225013 (YA, TS, RS), JP23wm0225022 (MS, MY, YH, TS, RS), JP23gm1610003, JP23fk0108642, JP23fk0108665, JP23fk0108683, JP23wm0325037, and JP23wm0225022 (MS), JP23fk0108608, JP23wm0125007, JP23wm0225022, JP23wm0325054, JP23gm1610003, JP23gm1610007, and JP23fk0108673 (YH). The funders had no role in the study design, data collection and analysis, interpretation of data, decision to publish, or preparation of the manuscript.