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Applied and environmental microbiology2023; 89(8); e0037123; doi: 10.1128/aem.00371-23

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

Abstract: 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.
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Publication Date: 2023-08-14 PubMed ID: 37578374PubMed Central: PMC10467340DOI: 10.1128/aem.00371-23Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates the frequency and distribution of the fos operon in antimicrobial-resistant Escherichia coli isolates. The fos operon enables bacteria to utilize short-chain fructooligosaccharides to survive in certain environments. The researchers found that fos operon and potentially resistance-bearing plasmids are not confined to a single group of sources, suggesting further study is needed into its role in antibiotic resistance.

Research Methods and Process

  • To start, this research involved screening a collection of 11,538 antimicrobial-resistant E. coli isolates. These were from a variety of sources.
  • The researchers were looking particularly for the fos gene, which encodes the transporter for short-chain fructooligosaccharides (scFOS). These are sugars that a sub-group of E.coli can eat to survive when other food sources are scarce.
  • Out of the total collection, 307 isolates were found to be positive for the fos gene.

Results and Findings

  • 80% of the fos-positive isolates came from sources that were not previously associated with this gene specifically. These sources included human, wastewater, and various animals.
  • Whole-genome sequencing was conducted on 237 of these isolates. The fos operon was detected in 163 of them.
  • In the remaining 74 isolates, the fos operon was carried by plasmids. Plasmids are small DNA molecules within a cell that are physically separated from chromosomal DNA and can replicate independently. They are most commonly found in bacteria.
  • The fos operon in these 74 isolates were associated with different incompatibility (Inc) groups, including the IncHI1, IncF-type, IncK2, IncI1, and IncY families.
  • Long-read sequencing of representative plasmids showed that fos genes were located together with antibiotic resistance genes (ARGs) in a number of Inc families.

Conclusions and Implications

  • The research demonstrated that the fos operon capable of enabling bacteria to survive in certain challenging environments is not restricted to one group of plasmids or sources.
  • Importantly, there were several instances where the fos genes were located on the same plasmids as antibiotic resistance genes, suggesting that plasmids carrying the fos operon may contribute to the spread of antibiotic resistance.
  • The spread and distribution of the fos operon, given its potential link to antibiotic resistance, should not be overlooked in future research and efforts to control antimicrobial resistance.

Cite This Article

APA
Nohejl T, Palkovicova J, Nesporova K, Valcek A, Lausova J, Dolejska M. (2023). Broad-Host Dissemination of Plasmids Coharboring the fos Operon for Fructooligosaccharide Metabolism with Antibiotic Resistance Genes. Appl Environ Microbiol, 89(8), e0037123. https://doi.org/10.1128/aem.00371-23

Publication

Applied and environmental microbiology
ISSN: 1098-5336
NlmUniqueID: 7605801
Country: United States
Language: English
Volume: 89
Issue: 8
Pages: e0037123
PII: e00371-23

Researcher Affiliations

Nohejl, Tomas
  • Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary Sciences Brno, Brno, Czech Republic.
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
Palkovicova, Jana
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
Nesporova, Kristina
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
Valcek, Adam
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
  • Microbial Resistance and Drug Discovery, VIB-VUB Center for Structural Biology, VIB, Flanders Institute for Biotechnology, Brussels, Belgium.
  • Structural Biology Brussels, Vrije Universiteit Brussel (VUB), Brussels, Belgium.
Lausova, Jarmila
  • Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary Sciences Brno, Brno, Czech Republic.
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
Dolejska, Monika
  • Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary Sciences Brno, Brno, Czech Republic.
  • CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
  • Department of Clinical Microbiology and Immunology, Institute of Laboratory Medicine, The University Hospital Brno, Brno, Czech Republic.
  • Faculty of Medicine, Biomedical Center, Charles University, Pilsen, Czech Republic.

MeSH Terms

  • Animals
  • Horses
  • Humans
  • Anti-Bacterial Agents / pharmacology
  • Escherichia coli
  • Plasmids / genetics
  • Escherichia coli Infections / microbiology
  • Enterobacteriaceae
  • Drug Resistance, Microbial
  • Operon
  • Microbial Sensitivity Tests
  • beta-Lactamases / genetics

Conflict of Interest Statement

The authors declare no conflict of interest.

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