Genomics, biofilm formation and infection of bladder epithelial cells in potentially uropathogenic Escherichia coli (UPEC) from animal sources and human urinary tract infections (UTIs) further support food-borne transmission

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  • Vanesa García
  • Luz Lestón
  • Ana Parga
  • Isidro García-Meniño
  • Javier Fernández
  • Ana Otero
  • Olsen, John Elmerdahl
  • Ana Herrero-Fresno
  • Azucena Mora

Escherichia coli is the main cause of urinary tract infections (UTI). While genomic comparison of specific clones recovered from animals, and human extraintestinal infections show high identity, studies demonstrating the uropathogenicity are lacking. In this study, comparative genomics combined with bladder-cell and biofilm formation assays, were performed for 31 E. coli of different origins: 7 from meat (poultry, beef, and pork); 2 from avian-farm environment; 12 from human uncomplicated UTI, uUTI; and 10 from human complicated UTI, cUTI. These isolates were selected based on their genetic uropathogenic (UPEC) status and phylogenetic background. In silico analysis revealed similar virulence-gene profiles, with flagella, type 1 and curli fimbriae, outer-membrane proteins (agn43, ompT, iha), and iron-uptake (iutA, entA, and fyuA) associated-traits as the most prevalent (>65%). In bladder-cell assays, moderate to strong values of association (83%, 60%, 77.8%) and invasion (0%, 70%, 55.5%) were exhibited by uUTI, cUTI, and animal-derived isolates, respectively. Of interest, uUTI isolates exhibited a significantly lower invasive capacity than cUTI isolates (p < 0.05). All isolates but one produced measurable biofilm. Notably, 1 turkey meat isolate O11:H6-F-ST457, and 2 cUTI isolates of the pandemic lineages O83:H42-F-ST1485-CC648 and O25b:H4-B2-ST131, showed strong association, invasion and biofilm formation. These isolates showed common carriage of type 1 fimbriae and csg operons, toxins (hlyF, tsh), iron uptake systems (iutA, entA, iroN), colicins, protectins (cvaC, iss, kpsM, traT), ompT, and malX. In summary, the similar in vitro behaviour found here for certain E. coli clones of animal origin would further reinforce the role of food-producing animals as a potential source of UPEC. Bladder-cell infection assays, combined with genomics, might be an alternative to in vivo virulence models to assess uropathogenicity.

OriginalsprogEngelsk
Artikelnummer100558
TidsskriftOne Health
Vol/bind16
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
This study was supported by the projects and funds PID2019-104439RB-C21/AEI/10.13039/501100011033 from the Agencia Estatal de Investigación (AEI, Spain), co-funded by the European Regional Development Fund of the European Union : a Way to Make Europe (ERDF); ED431C 2021/11 and ED431B 2020/13 from the Consellería de Cultura, Educación e Ordenación Universitaria ( Xunta de Galicia ) and ERDF. GRUPIN IDI/2022/000033 by the Regional Ministry of Science of Asturias ( IDI/2022/000033 ). Co-funded by Independent Research Found Denmark (grant number 4184–00050 ) to the project Combining non-essential metabolic targets into suitable targets for control of uropathogenic Escherichia coli.

Funding Information:
This study was supported by the projects and funds PID2019-104439RB-C21/AEI/10.13039/501100011033 from the Agencia Estatal de Investigación (AEI, Spain), co-funded by the European Regional Development Fund of the European Union: a Way to Make Europe (ERDF); ED431C 2021/11 and ED431B 2020/13 from the Consellería de Cultura, Educación e Ordenación Universitaria (Xunta de Galicia) and ERDF. GRUPIN IDI/2022/000033 by the Regional Ministry of Science of Asturias (IDI/2022/000033). Co-funded by Independent Research Found Denmark (grant number 4184–00050) to the project Combining non-essential metabolic targets into suitable targets for control of uropathogenic Escherichia coli.VG and IG-M acknowledge the Consellería de Cultura, Educación e Ordenación Universitaria, Xunta de Galicia for their post-doctoral grants (Grant Number ED481D-2022-012 and ED481B-2021-006, respectively). LL acknowledges the Ministry of Education of Spain for her pre-doctoral Grant FPU19/01127. AP acknowledges the Regional Government of Galicia for her pre-doctoral grant (ED481A-2019/194). The authors would like to thank AllGenetics & Biology SL (www.allgenetics.eu) for supporting us with the genomic analysis service.

Funding Information:
VG and IG-M acknowledge the Consellería de Cultura , Educación e Ordenación Universitaria , Xunta de Galicia for their post-doctoral grants (Grant Number ED481D-2022-012 and ED481B-2021-006 , respectively). LL acknowledges the Ministry of Education of Spain for her pre-doctoral Grant FPU19/01127 . AP acknowledges the Regional Government of Galicia for her pre-doctoral grant ( ED481A-2019/194 ).

Publisher Copyright:
© 2023 The Author(s)

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