Complete genetic characterization of carbapenem-resistant Acinetobacter johnsonii, co-producing NDM-1, OXA-58, and PER-1 in a patient source

Front Cell Infect Microbiol. 2023 Aug 25:13:1227063. doi: 10.3389/fcimb.2023.1227063. eCollection 2023.

Abstract

The emergence of carbapenemase-producing Acinetobacter spp. has been widely reported and become a global threat. However, carbapenem-resistant A. johnsonii strains are relatively rare and without comprehensive genetic structure analysis, especially for isolates collected from human specimen. Here, one A. johnsonii AYTCM strain, co-producing NDM-1, OXA-58, and PER-1 enzymes, was isolated from sputum in China in 2018. Antimicrobial susceptibility testing showed that it was resistant to meropenem, imipenem, ceftazidime, ciprofloxacin, and cefoperazone/sulbactam. Whole-genome sequencing and bioinformatic analysis revealed that it possessed 11 plasmids. bla OXA-58 and bla PER-1 genes were located in the pAYTCM-1 plasmid. Especially, a complex class 1 integron consisted of a 5' conserved segment (5' CS) and 3' CS, which was found to carry sul1, arr-3, qnrVC6, and bla PER-1 cassettes. Moreover, the bla NDM-1 gene was located in 41,087 conjugative plasmids and was quite stable even after 70 passages under antibiotics-free conditions. In addition, six prophage regions were identified. Tracking of closely related plasmids in the public database showed that pAYTCM-1 was similar to pXBB1-9, pOXA23_010062, pOXA58_010030, and pAcsw19-2 plasmids, which were collected from the strains of sewage in China. Concerning the pAYTCM-3 plasmids, results showed that strains were collected from different sources and their hosts were isolated from various countries, such as China, USA, Japan, Brazil, and Mexico, suggesting that a wide spread occurred all over the world. In conclusion, early surveillance is warranted to avoid the extensive spread of this high-risk clone in the healthcare setting.

Keywords: Acinetobacter johnsonii; NDM-1; OXA-58; PER-1; carbapenem resistance; integron.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinetobacter* / genetics
  • Carbapenems* / pharmacology
  • Genes, Regulator
  • Humans
  • Transcription Factors

Substances

  • Carbapenems
  • beta-lactamase NDM-1
  • Transcription Factors

Supplementary concepts

  • Acinetobacter johnsonii

Grants and funding

This work was supported by the Medical Health Science and Technology Project of Zhejiang Provincial Health Commission (2023KY1270, 2022RC278); Natural Science Foundation of Zhejiang Province (LQ19H160002), Quzhou technology projects, China (2019K36); and Zhejiang Province Traditional Chinese Medicine Science and Technology Project (2023ZL729).