Housefly (Musca domestica) and Blow Fly (Protophormia terraenovae) as Vectors of Bacteria Carrying Colistin Resistance Genes

Abstract

Flies have the capacity to transfer pathogens between different environments, acting as one of the most important vectors of human diseases worldwide. In this study, we trapped flies on a university campus and tested them for mobile resistance genes against colistin, a last-resort antibiotic in human medicine for treating clinical infections caused by multidrug-resistant Gram-negative bacteria. Quantitative PCR assays we developed showed that 34.1% of <i>Musca domestica</i> (86/252) and 51.1% of <i>Protophormia terraenovae</i> (23/45) isolates were positive for the <i>mcr-1</i> gene, 1.2% of <i>M. domestica</i> (3/252) and 2.2% of <i>P. terraenovae</i> (2.2%, 1/45) isolates were positive for <i>mcr-2</i>, and 5.2% of <i>M. domestica</i> (13/252) and 44.4% of <i>P. terraenovae</i> (20/45) isolates were positive for <i>mcr-3</i> Overall, 4.8% (9/189) of bacteria isolated from the flies were positive for the <i>mcr-1</i> gene (<i>Escherichia coli</i>: 8.3%, 4/48; <i>Enterobacter cloacae</i>: 12.5%, 1/8; <i>Providencia alcalifaciens</i>: 11.8%, 2/17; <i>Providencia stuartii</i>: 4.9%, 2/41), while none were positive for <i>mcr-2</i> and <i>mcr-3</i> Four <i>mcr-1</i>-positive isolates (two <i>P. stuartii</i> and two <i>P. alcalifaciens</i>) from blow flies trapped near a dumpster had a MIC for colistin above 4 mg/ml. This study reports <i>mcr-1</i> carriage in <i>Providencia</i> spp. and detection of <i>mcr-2</i> and <i>mcr-3</i> after their initial identification in Belgium and China, respectively. This study suggests that flies might contribute significantly to the dissemination of bacteria, carrying these genes into a large variety of ecological niches. Further studies are warranted to explore the roles that flies might play in the spread of colistin resistance genes.<b>IMPORTANCE</b> Antimicrobial resistance is recognized as one of the most serious global threats to human health. An option for treatment of the Gram-negative ESKAPE (<i>Enterococcus faecium</i>, <i>Staphylococcus aureus</i>, <i>Klebsiella pneumoniae</i>, <i>Acinetobacter baumannii</i>, <i>Pseudomonas aeruginosa</i>, and <i>Enterobacter</i> species) bacteria with multiple drug resistance was the reintroduction of the older antibiotic colistin. However, a mobile colistin resistance gene (<i>mcr-1</i>) has recently been found to occur widely; very recently, two other colistin resistance genes (<i>mcr-2</i> and <i>mcr-3</i>) have been identified in Belgium and China, respectively. In this study, we report the presence of colistin resistance genes in flies. This study also reports the carriage of colistin resistance genes in the genus <i>Providencia</i> and detection of <i>mcr-2</i> and <i>mcr-3</i> after their initial identification. This study will stimulate more in-depth studies to fully elucidate the transmission mechanisms of the colistin resistance genes and their interaction.