Emergence of blaIMI-2- and blaIMI-16-Producing Enterobacter asburiae in the Aquaculture Environment of Jiangsu, China

Abstract

Carbapenem-resistant Enterobacteriaceae strains have emerged as a serious threat to global public health. In recent years, bla_IMI, a carbapenemase gene that drew less attention before, has been increasingly detected in both clinical and environmental settings. However, the environmental distribution and transmission of bla_IMI, especially in aquaculture, require systematic investigation. In this study, the bla_IMI gene was detected in fish (n = 1), sewage (n = 1), river water (n = 1), and aquaculture pond water samples (n = 17) collected from Jiangsu, China, demonstrating a relatively high sample-positive ratio of 12.4% (20/161). Thirteen bla_IMI-2- or bla_IMI-16-carrying Enterobacter asburiae strains were isolated from bla_IMI-positive samples of aquatic products and aquaculture ponds. We also identified a novel transposon (Tn7441) carrying bla_IMI-16 and a conserved region containing several truncated insertion sequence (IS) elements harboring bla_IMI-2, all of which may play important roles in bla_IMI mobilization. The occurrence of bla_IMI-carrying Enterobacter asburiae in aquaculture-related water samples and fish samples highlights the risk of transmission of bla_IMI-carrying strains through the food chain and the need for effective measures to prevent further dissemination. IMPORTANCE IMI carbapenemases have been detected in clinical isolates of many bacterial species with systemic infection and cause a further burden on clinical treatment in China, but their source and distribution are still unclear. The study systematically investigated the distribution and transmission of the bla_IMI gene in aquaculture-related water bodies and aquatic products in Jiangsu Province, China, which is famous for its rich water resources and developed aquaculture industry. The relatively high prevalence of bla_IMI in aquaculture samples and the identification of novel mobile elements harboring bla_IMI enhance our knowledge of bla_IMI gene distribution and highlight the public health risk and urgency of surveillance of aquaculture water systems in China.

Keywords: Enterobacter asburiae; aquaculture environment; blaIMI; novel transposon Tn7441.

FIG 1

Comparative analysis of bla_IMI-2-carrying plasmids. (a) Sequence comparison of two completely sequenced bla_IMI-2-carrying plasmids, pCFB52_IMI and pCW353_IMI. (b) Gene environment of bla_IMI-2 in different plasmids. Plasmid information is listed on the left side. Open reading frames (ORFs) are indicated by arrows. Blue arrows indicate the antimicrobial resistance gene, bla_IM, and its regulator protein gene, bla_IMI-R. Red arrows indicate the insertion sequences. Gray arrows indicate hypothetical proteins. Orange arrows indicate other genes. Identical regions are highlighted in light blue (>95% similarity).

FIG 2

Comparative analysis of bla_IMI-16-carrying plasmids. (a) BRIG comparison of pCW1_IMI with other bla_IMI-carrying plasmids. The innermost rings show GC skew (purple/green) and GC content (black). Each ring represents the plasmid indicated by the corresponding color. The location of the bla_IMI gene is indicated with black text and orange shading. (b) Genetic structure of bla_IMI-16 with different bla_IMI-carrying plasmids. Plasmid information is listed on the right side. ORFs are indicated by arrows. Blue arrows indicate the antimicrobial resistance gene bla_IMI and its regulator protein gene bla_IMI-R. Red arrows indicate the insertion sequences. Gray arrows indicate hypothetical proteins. Orange arrows indicate other genes. Identical regions are highlighted in light blue (>89% similarity).