Broad-Host Dissemination of Plasmids Coharboring the Operon for Fructooligosaccharide Metabolism with Antibiotic Resistance Genes.

The operon encoding short-chain fructooligosaccharide (scFOS) utilization enables bacteria of the family to grow and be sustained in environments where they would struggle to survive. Despite several cases of the detection of the operon in isolates of avian and equine origins, its global distribution in bacterial genomes remains unknown. The presence of the plasmid-harbored operon among resistant bacteria may promote the spread of antibiotic resistance. A collection of 11,538 antimicrobial-resistant isolates from various sources was screened for the gene encoding the scFOS transporter. Out of 307 -positive isolates, 80% of them originated from sources not previously linked to (humans, wastewater, and animals). The chromosomally harbored operon was detected in 163/237 isolates subjected to whole-genome sequencing. In the remaining 74 isolates, the operon was carried by plasmids. Further analyses focusing on the isolates with a plasmid-harbored operon showed that the operon was linked to various incompatibility (Inc) groups, including the IncHI1, IncF-type, IncK2, IncI1, and IncY families. Long-read sequencing of representative plasmids showed the colocalization of genes with antibiotic resistance genes (ARGs) in IncHI1 (containing a multidrug resistance region), IncK2 (), IncI1 [ and (A)], and IncY [, , , and (A)] plasmids, while IncF-type plasmids had no ARGs but coharbored virulence-associated genes. Despite the differences in the locations and structures of the operons, all isolates except one were proven to utilize scFOSs. In this study, we show that the operon and its spread are not strictly bound to one group of plasmids, and therefore, it should not be overlooked. It was believed that members of the family are unable to grow under conditions with short-chain fructooligosaccharides as the only source of carbon. Nevertheless, the first Escherichia coli isolate from chicken intestine was able to utilize these sugars owing to the chromosomally harbored operon. Studies on E. coli isolates from horses discovered the horizontal transfer of the operon on IncHI1 plasmids along with genes for antibiotic resistance. The first plasmid detected was pEQ1, originating from the feces of a hospitalized horse in the Czech Republic. Follow-up studies also revealed the dissemination of the IncHI1 plasmid-harbored operon in the Netherlands, Germany, Denmark, and France among healthy horses. Despite several cases of detection of the operon, its global distribution in bacterial genomes remains unknown. The operon possibly plays a role in the adaptation of plasmids among resistant bacteria and therefore may promote the spread of antibiotic resistance.