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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.
Publication Date: 2023-08-14 PubMed ID: 37578374PubMed Central: PMC10467340DOI: 10.1128/aem.00371-23Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

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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

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.

References

This article includes 39 references
  1. Grand E, Respondek F, Martineau C, Detilleux J, Bertrand G. Effects of short-chain fructooligosaccharides on growth performance of preruminant veal calves.. J Dairy Sci 2013 Feb;96(2):1094-101.
    doi: 10.3168/jds.2011-4949pubmed: 23200477google scholar: lookup
  2. Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in Bifidobacteria.. Genes Nutr 2011 Aug;6(3):285-306.
    doi: 10.1007/s12263-010-0206-6pmc: PMC3145055pubmed: 21484167google scholar: lookup
  3. Bornet FR, Brouns F, Tashiro Y, Duvillier V. Nutritional aspects of short-chain fructooligosaccharides: natural occurrence, chemistry, physiology and health implications.. Dig Liver Dis 2002 Sep;34 Suppl 2:S111-20.
    doi: 10.1016/S1590-8658(02)80177-3pubmed: 12408453google scholar: lookup
  4. Liu F, Li P, Chen M, Luo Y, Prabhakar M, Zheng H, He Y, Qi Q, Long H, Zhang Y, Sheng H, Zhou H. Fructooligosaccharide (FOS) and Galactooligosaccharide (GOS) Increase Bifidobacterium but Reduce Butyrate Producing Bacteria with Adverse Glycemic Metabolism in healthy young population.. Sci Rep 2017 Sep 18;7(1):11789.
    doi: 10.1038/s41598-017-10722-2pmc: PMC5603605pubmed: 28924143google scholar: lookup
  5. Chouikha I, Germon P, Brée A, Gilot P, Moulin-Schouleur M, Schouler C. A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence.. J Bacteriol 2006 Feb;188(3):977-87.
  6. Porcheron G, Chanteloup NK, Trotereau A, Brée A, Schouler C. Effect of fructooligosaccharide metabolism on chicken colonization by an extra-intestinal pathogenic Escherichia coli strain.. PLoS One 2012;7(4):e35475.
  7. Dolejska M, Villa L, Minoia M, Guardabassi L, Carattoli A. Complete sequences of IncHI1 plasmids carrying blaCTX-M-1 and qnrS1 in equine Escherichia coli provide new insights into plasmid evolution.. J Antimicrob Chemother 2014 Sep;69(9):2388-93.
    doi: 10.1093/jac/dku172pubmed: 24862095google scholar: lookup
  8. Valcek A, Sismova P, Nesporova K, Overballe-Petersen S, Bitar I, Jamborova I, Kant A, Hrabak J, Wagenaar JA, Madec JY, Damborg P, van Duijkeren E, Ewers C, Hordijk J, Hasman H, Brouwer MSM, Dolejska M. Horsing around: Escherichia coli ST1250 of equine origin harbouring epidemic IncHI1/ST9 plasmid with bla (CTX-M-1) and an operon for short-chain fructooligosaccharides metabolism.. Antimicrob Agents Chemother 2023 May 1;65(5).
    doi: 10.1128/AAC.02556-20pmc: PMC8092906pubmed: 33619063google scholar: lookup
  9. de Lagarde M, Larrieu C, Praud K, Lallier N, Trotereau A, Sallé G, Fairbrother JM, Schouler C, Doublet B. Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene bla(CTX-M-1) and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France.. Int J Antimicrob Agents 2020 Jun;55(6):105936.
  10. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile Genetic Elements Associated with Antimicrobial Resistance.. Clin Microbiol Rev 2018 Oct;31(4).
    doi: 10.1128/CMR.00088-17pmc: PMC6148190pubmed: 30068738google scholar: lookup
  11. Respondek F, Goachet AG, Julliand V. Effects of dietary short-chain fructooligosaccharides on the intestinal microflora of horses subjected to a sudden change in diet.. J Anim Sci 2008 Feb;86(2):316-23.
    doi: 10.2527/jas.2006-782pubmed: 17940163google scholar: lookup
  12. Respondek F, Myers K, Smith TL, Wagner A, Geor RJ. Dietary supplementation with short-chain fructo-oligosaccharides improves insulin sensitivity in obese horses.. J Anim Sci 2011 Jan;89(1):77-83.
    doi: 10.2527/jas.2010-3108pubmed: 20870952google scholar: lookup
  13. Literak I, Dolejska M, Rybarikova J, Cizek A, Strejckova P, Vyskocilova M, Friedman M, Klimes J. Highly variable patterns of antimicrobial resistance in commensal Escherichia coli isolates from pigs, sympatric rodents, and flies.. Microb Drug Resist 2009 Sep;15(3):229-37.
    doi: 10.1089/mdr.2009.0913pubmed: 19728783google scholar: lookup
  14. Cormier AC, Chalmers G, Zamudio R, Mulvey MR, Mather AE, Boerlin P. Diversity of blaCTX-M-1-carrying plasmids recovered from Escherichia coli isolated from Canadian domestic animals.. PLoS One 2022;17(3):e0264439.
  15. Palomino A, Gewurz D, DeVine L, Zajmi U, Moralez J, Abu-Rumman F, Smith RP, Lopatkin AJ. Metabolic genes on conjugative plasmids are highly prevalent in Escherichia coli and can protect against antibiotic treatment.. ISME J 2023 Jan;17(1):151-162.
    doi: 10.1038/s41396-022-01329-1pmc: PMC9750983pubmed: 36261510google scholar: lookup
  16. Caza M, Garénaux A, Lépine F, Dozois CM. Catecholate siderophore esterases Fes, IroD and IroE are required for salmochelins secretion following utilization, but only IroD contributes to virulence of extra-intestinal pathogenic Escherichia coli.. Mol Microbiol 2015 Aug;97(4):717-32.
    doi: 10.1111/mmi.13059pubmed: 25982934google scholar: lookup
  17. Gérard F, Pradel N, Wu LF. Bactericidal activity of colicin V is mediated by an inner membrane protein, SdaC, of Escherichia coli.. J Bacteriol 2005 Mar;187(6):1945-50.
  18. Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B, Guerra B, Mevius DJ, Hordijk J. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae.. J Antimicrob Chemother 2018 May 1;73(5):1121-1137.
    doi: 10.1093/jac/dkx488pubmed: 29370371google scholar: lookup
  19. Jiang N, Dillon FM, Silva A, Gomez-Cano L, Grotewold E. Rhamnose in plants - from biosynthesis to diverse functions.. Plant Sci 2021 Jan;302:110687.
  20. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
  21. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.. J Comput Biol 2012 May;19(5):455-77.
    doi: 10.1089/cmb.2012.0021pmc: PMC3342519pubmed: 22506599google scholar: lookup
  22. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing.. Microb Genom 2017 Oct;3(10):e000132.
    doi: 10.1099/mgen.0.000132pmc: PMC5695209pubmed: 29177090google scholar: lookup
  23. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads.. PLoS Comput Biol 2017 Jun;13(6):e1005595.
  24. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs.. Nat Biotechnol 2019 May;37(5):540-546.
    doi: 10.1038/s41587-019-0072-8pubmed: 30936562google scholar: lookup
  25. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads.. Genome Res 2017 May;27(5):737-746.
    doi: 10.1101/gr.214270.116pmc: PMC5411768pubmed: 28100585google scholar: lookup
  26. Lee JY, Kong M, Oh J, Lim J, Chung SH, Kim JM, Kim JS, Kim KH, Yoo JC, Kwak W. Comparative evaluation of Nanopore polishing tools for microbial genome assembly and polishing strategies for downstream analysis.. Sci Rep 2021 Oct 20;11(1):20740.
    doi: 10.1038/s41598-021-00178-wpmc: PMC8528807pubmed: 34671046google scholar: lookup
  27. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement.. PLoS One 2014;9(11):e112963.
  28. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform.. Bioinformatics 2009 Jul 15;25(14):1754-60.
  29. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. VFDB: a reference database for bacterial virulence factors.. Nucleic Acids Res 2005 Jan 1;33(Database issue):D325-8.
    doi: 10.1093/nar/gki008pmc: PMC539962pubmed: 15608208google scholar: lookup
  30. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, Møller Aarestrup F, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.. Antimicrob Agents Chemother 2014 Jul;58(7):3895-903.
    doi: 10.1128/AAC.02412-14pmc: PMC4068535pubmed: 24777092google scholar: lookup
  31. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, Philippon A, Allesoe RL, Rebelo AR, Florensa AF, Fagelhauer L, Chakraborty T, Neumann B, Werner G, Bender JK, Stingl K, Nguyen M, Coppens J, Xavier BB, Malhotra-Kumar S, Westh H, Pinholt M, Anjum MF, Duggett NA, Kempf I, Nykäsenoja S, Olkkola S, Wieczorek K, Amaro A, Clemente L, Mossong J, Losch S, Ragimbeau C, Lund O, Aarestrup FM. ResFinder 4.0 for predictions of phenotypes from genotypes.. J Antimicrob Chemother 2020 Dec 1;75(12):3491-3500.
    doi: 10.1093/jac/dkaa345pmc: PMC7662176pubmed: 32780112google scholar: lookup
  32. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences.. Nucleic Acids Res 2006 Jan 1;34(Database issue):D32-6.
    doi: 10.1093/nar/gkj014pmc: PMC1347377pubmed: 16381877google scholar: lookup
  33. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH. CDD: NCBI's conserved domain database.. Nucleic Acids Res 2015 Jan;43(Database issue):D222-6.
    doi: 10.1093/nar/gkሡpmc: PMC4383992pubmed: 25414356google scholar: lookup
  34. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan genome analysis.. Bioinformatics 2015 Nov 15;31(22):3691-3.
  35. Seemann T. Prokka: rapid prokaryotic genome annotation.. Bioinformatics 2014 Jul 15;30(14):2068-9.
    doi: 10.1093/bioinformatics/btu153pubmed: 24642063google scholar: lookup
  36. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.. Bioinformatics 2006 Nov 1;22(21):2688-90.
    doi: 10.1093/bioinformatics/btl446pubmed: 16928733google scholar: lookup
  37. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation.. Bioinformatics 2007 Jan 1;23(1):127-8.
    doi: 10.1093/bioinformatics/btl529pubmed: 17050570google scholar: lookup
  38. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons.. BMC Genomics 2011 Aug 8;12:402.
    doi: 10.1186/1471-2164-12-402pmc: PMC3163573pubmed: 21824423google scholar: lookup
  39. Gilchrist CLM, Chooi YH. clinker & clustermap.js: automatic generation of gene cluster comparison figures.. Bioinformatics 2021 Aug 25;37(16):2473-2475.

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