Introduction of the transmissible mobile colistin resistance genes mcr-3 and mcr-9 to the USA via imported seafood.

Abstract

The emergence and global dissemination of the mobile colistin resistance genes (mcr) threaten the efficacy of colistin, a high-priority, critically important antibiotic that is used to treat complicated infections with multidrug-resistant Gram-negative bacteria in humans. The occurrence of mcr in the USA has been suggested to be relatively limited, particularly in bacteria associated with domestic foods and food animals. This is because colistin has neither been marketed nor approved for use in agriculture in the USA. However, mcr-carrying bacteria can occur on foods imported from countries where these genes might be relatively more prevalent. Yet, studies on mcr in vulnerable imported foods in the USA are lacking. To address this gap in knowledge, we assessed the role of imported seafood as a potential carrier of mcr genes to the USA. Imported seafood samples were aseptically collected from eight major retail stores across Georgia, USA. In-depth analyses revealed the occurrence of mcr-9 in bacteria isolated from imported shrimp samples. The mcr-9-carrying bacteria were identified as Serratia nevei, a newly described species that belongs to the Serratia marcescens complex. The mcr-9 in the S. nevei isolates was carried on IncHI2 plasmids that were transferable and conferred colistin resistance to naïve Escherichia coli. Further analysis identified a chromosomal mcr-3.17 in Aeromonas salmonicida isolated from imported scallops. All the mcr-carrying isolates harbored other important antibiotic resistance genes. Taken together, our data showed that imported seafood, specifically shrimps, might be an overlooked source contributing to the introduction and spread of transmissible colistin resistance genes in the USA.

Importance: Colistin, an important antibiotic, is used to treat certain bacterial infections in humans that can be severe and/or life-threatening. However, these bacteria can acquire the mobile colistin resistance (mcr) genes and become resistant to this antibiotic. Plasmid-borne mcr can jump between bacterial species, spreading in bacteria across a variety of hosts and niches. Therefore, monitoring the spread of mcr is critical to maintain the efficacy of colistin. In the USA, the occurrence of mcr in domestically produced food is thought to be limited. In this study, we showed that mcr can be carried into the USA by bacteria on imported seafood. A specific gene, mcr-9, was located on a plasmid that could be transferred to other bacteria. Therefore, imported seafood can be an overlooked source of mcr in the USA. It is important to monitor and assess mcr in imported seafood to control the proliferation of colistin resistance in the USA.