Genomic Analysis of a Highly Virulent NDM-1-Producing Escherichia coli ST162 Infecting a Pygmy Sperm Whale (Kogia breviceps) in South America

Carbapenemase-producing Enterobacterales are rapidly spreading and adapting to different environments beyond hospital settings. During COVID-19 lockdown, a carbapenem-resistant NDM-1-positive Escherichia coli isolate (BA01 strain) was recovered from a pygmy sperm whale (Kogia breviceps), which was found stranded on the southern coast of Brazil. BA01 strain belonged to the global sequence type (ST) 162 and carried the bla(NDM-1), besides other medically important antimicrobial resistance genes. Additionally, genes associated with resistance to heavy metals, biocides, and glyphosate were also detected. Halophilic behavior (tolerance to > 10% NaCl) of BA01 strain was confirmed by tolerance tests of NaCl minimal inhibitory concentration, whereas halotolerance associated genes katE and nhaA, which encodes for catalase and Na+/H+ antiporter cytoplasmic membrane, respectively, were in silico confirmed. Phylogenomics clustered BA01 with poultry- and human-associated ST162 lineages circulating in European and Asian countries. Important virulence genes, including the astA (a gene encoding an enterotoxin associated with human and animal infections) were detected, whereas in vivo experiments using the Galleria mellonella infection model confirmed the virulent behavior of the BA01 strain. WHO critical priority carbapenemase-producing pathogens in coastal water are an emerging threat that deserves the urgent need to assess the role of the aquatic environment in its global epidemiology.

Automated summary

A carbapenem-resistant NDM-1-positive Escherichia coli isolate was recovered from a stranded pygmy sperm whale in Brazil. The isolate carried multiple antimicrobial resistance genes, as well as genes associated with heavy metal and biocide resistance. It exhibited halotolerance and virulent behavior, and was closely related to poultry- and human-associated lineages circulating in Europe and Asia. The presence of carbapenemase-producing pathogens in coastal water poses an emerging threat that requires urgent assessment of the role of the aquatic environment in their global epidemiology.