Hidden Resistances: How Routine Whole-Genome Sequencing Uncovered an Otherwise Undetected bla NDM-1 Gene in Vibrio alginolyticus from Imported Seafood

Abstract

Carbapenems are last-line antimicrobials, vital for use in human medicine. Antimicrobial resistance determinants such as bla NDM (New Delhi metallo-β-lactamase producing) genes conferring resistance to the carbapenem class of antimicrobials, are typically found in Enterobacterales (first described in 2009 from a Klebsiella pneumoniae isolate). Vibrio alginolyticus causes vibriosis of marine vertebrates, invertebrates, and humans, and while there have been several reports of multidrug resistance in V. alginolyticus , carbapenem resistance is rare. V. alginolyticus strain AUSMDU00064140 was isolated in Melbourne, Australia, from imported prawns. Routine genomic surveillance detected the presence of a full-length bla NDM-1 gene, subsequently shown to be collocated with additional acquired antimicrobial resistance genes on a resistance cassette on the largest chromosome, flanked by mobilization gene annotations. Comparisons to a previously described V. alginolyticus plasmid, pC1349, revealed differing gene content and arrangements between the resistance cassettes. Phylogenetic analysis was performed against a local and global data set ( n = 109), demonstrating that AUSMDU00064140 was distinct and did not cluster with any other strains. Despite the presence of the complete bla NDM-1 gene and positive phenotypic assays for carbapenemase production, carbapenem MICs were low (meropenem MIC ≤0.5 mg/liter). However, it is still possible that this gene may be transferred to another species in the environment or a host, causing phenotypic carbapenem resistance and presenting a risk of great public health concern. IMPORTANCE Carbapenems are last-line antimicrobials, vital for use in human medicine. Antimicrobial resistance determinants such as bla NDM (New Delhi metallo-β-lactamase producing) genes conferring resistance to the carbapenem class of antimicrobials, are typically found in Enterobacterales (first described in 2009 from a Klebsiella pneumoniae isolate). Our study shows that Vibrio alginolyticus isolated from cooked prawn is able to harbor antimicrobial resistance (AMR) genes of public health concern, specifically a chromosomally located bla NDM-1 gene, and there is the potential for transmission of resistance genes. This may be linked with antimicrobial use in low- and middle-income settings, which has typically been high, unregulated, or not reported. Many countries, including Thailand, have implemented national strategic plans to incorporate the World Health Organization (WHO)’s Global Action Plan (2015) recommendations of a global One Health approach, including increased resources for surveillance of antimicrobial usage and AMR; however, efficient antimicrobial surveillance systems incorporating genomic and phenotypic testing of isolates are still lacking in many jurisdictions.