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Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli

BACKGROUND: Escherichia coli biofilm formation has mostly been assessed in specific pathogenic E. coli groups. Here, we assessed the early biofilm formation (EBF), i.e., adhesion stage, using the BioFilm Ring Test(®) on 394 E. coli clinical isolates (EC) [196 consecutively isolated (CEC) in 2016 and...

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Autores principales: Flament-Simon, Saskia-Camille, Duprilot, Marion, Mayer, Noémie, García, Vanesa, Alonso, María Pilar, Blanco, Jorge, Nicolas-Chanoine, Marie-Hélène
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6555128/
https://www.ncbi.nlm.nih.gov/pubmed/31214138
http://dx.doi.org/10.3389/fmicb.2019.01183
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author Flament-Simon, Saskia-Camille
Duprilot, Marion
Mayer, Noémie
García, Vanesa
Alonso, María Pilar
Blanco, Jorge
Nicolas-Chanoine, Marie-Hélène
author_facet Flament-Simon, Saskia-Camille
Duprilot, Marion
Mayer, Noémie
García, Vanesa
Alonso, María Pilar
Blanco, Jorge
Nicolas-Chanoine, Marie-Hélène
author_sort Flament-Simon, Saskia-Camille
collection PubMed
description BACKGROUND: Escherichia coli biofilm formation has mostly been assessed in specific pathogenic E. coli groups. Here, we assessed the early biofilm formation (EBF), i.e., adhesion stage, using the BioFilm Ring Test(®) on 394 E. coli clinical isolates (EC) [196 consecutively isolated (CEC) in 2016 and 198 ESBL-producing E. coli (ESBLEC) isolated in 2015]. Then, biofilm-forming ability was contrasted with phylogroups, clonotypes (fumC-fimH), and sequence types (STs), all being used to define clones, virulence factors (VF), and FimB. RESULT: According to both biofilm production levels at 2, 3, and 5 h, and EBF kinetics over 5 h, CEC and ESBLEC isolates segregated into three EBF groups: strong (G1), moderate (G2), and weak (G3) producers. At 2 h, strong producers were more frequent among CEC (n = 28; 14.3%) than among ESBLEC (n = 8; 4%) (P = 0.0004). As CEC and ESBLEC isolates showed similar individual EBF kinetics in each group, a comparison of isolate features between each group was applied to gathered CEC and ESBLEC isolates after 2 h of incubation, 2 h being the most representative time point of the CEC and ESBLEC isolate segregation into the three groups. Phylogroup B2 displayed by 51.3% of the 394 isolates was more frequent in G1 (77.8%) than in G3 (47.6%) (P = 0.0006). The 394 isolates displayed 153 clones, of which 31 included at least three isolates. B2-CH14-2-ST127, B2-CH40-22-ST131, B2-CH52-5/14-ST141, and E-CH100-96-ST362 clones were associated with G1 (P < 0.03) and accounted for 41.7% of G1 isolates. B2-CH40-30-ST131 clone was associated with G3 (P < 0.0001) and accounted for 25.5% of G3 isolates. VF mean was higher among G1 than among G3 isolates (P < 0.001). FimB-P2 variant was associated with G1 (P = 0.0011) and FimB-P1 variant was associated with G3 (P = 0.0023). Clone, some VF, and FimB were associated with EBF, with clonal lineage being able to explain 72% of the variability of EBF. CONCLUSION: Among our 394 isolates, <10% are able to quickly and persistently produce high biofilm levels over 5 h. These isolates belong to a few clones previously described in various studies as dominant gut colonizers in mammalians and birds and comprised the B2-CH40-22-ST131 clone, i.e., the ancestor of the globally disseminated B2-CH40-30-ST131 clone that is the dominant clone among the weak biofilm producers.
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spelling pubmed-65551282019-06-18 Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli Flament-Simon, Saskia-Camille Duprilot, Marion Mayer, Noémie García, Vanesa Alonso, María Pilar Blanco, Jorge Nicolas-Chanoine, Marie-Hélène Front Microbiol Microbiology BACKGROUND: Escherichia coli biofilm formation has mostly been assessed in specific pathogenic E. coli groups. Here, we assessed the early biofilm formation (EBF), i.e., adhesion stage, using the BioFilm Ring Test(®) on 394 E. coli clinical isolates (EC) [196 consecutively isolated (CEC) in 2016 and 198 ESBL-producing E. coli (ESBLEC) isolated in 2015]. Then, biofilm-forming ability was contrasted with phylogroups, clonotypes (fumC-fimH), and sequence types (STs), all being used to define clones, virulence factors (VF), and FimB. RESULT: According to both biofilm production levels at 2, 3, and 5 h, and EBF kinetics over 5 h, CEC and ESBLEC isolates segregated into three EBF groups: strong (G1), moderate (G2), and weak (G3) producers. At 2 h, strong producers were more frequent among CEC (n = 28; 14.3%) than among ESBLEC (n = 8; 4%) (P = 0.0004). As CEC and ESBLEC isolates showed similar individual EBF kinetics in each group, a comparison of isolate features between each group was applied to gathered CEC and ESBLEC isolates after 2 h of incubation, 2 h being the most representative time point of the CEC and ESBLEC isolate segregation into the three groups. Phylogroup B2 displayed by 51.3% of the 394 isolates was more frequent in G1 (77.8%) than in G3 (47.6%) (P = 0.0006). The 394 isolates displayed 153 clones, of which 31 included at least three isolates. B2-CH14-2-ST127, B2-CH40-22-ST131, B2-CH52-5/14-ST141, and E-CH100-96-ST362 clones were associated with G1 (P < 0.03) and accounted for 41.7% of G1 isolates. B2-CH40-30-ST131 clone was associated with G3 (P < 0.0001) and accounted for 25.5% of G3 isolates. VF mean was higher among G1 than among G3 isolates (P < 0.001). FimB-P2 variant was associated with G1 (P = 0.0011) and FimB-P1 variant was associated with G3 (P = 0.0023). Clone, some VF, and FimB were associated with EBF, with clonal lineage being able to explain 72% of the variability of EBF. CONCLUSION: Among our 394 isolates, <10% are able to quickly and persistently produce high biofilm levels over 5 h. These isolates belong to a few clones previously described in various studies as dominant gut colonizers in mammalians and birds and comprised the B2-CH40-22-ST131 clone, i.e., the ancestor of the globally disseminated B2-CH40-30-ST131 clone that is the dominant clone among the weak biofilm producers. Frontiers Media S.A. 2019-05-31 /pmc/articles/PMC6555128/ /pubmed/31214138 http://dx.doi.org/10.3389/fmicb.2019.01183 Text en Copyright © 2019 Flament-Simon, Duprilot, Mayer, García, Alonso, Blanco and Nicolas-Chanoine. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Flament-Simon, Saskia-Camille
Duprilot, Marion
Mayer, Noémie
García, Vanesa
Alonso, María Pilar
Blanco, Jorge
Nicolas-Chanoine, Marie-Hélène
Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title_full Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title_fullStr Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title_full_unstemmed Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title_short Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in Escherichia coli
title_sort association between kinetics of early biofilm formation and clonal lineage in escherichia coli
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6555128/
https://www.ncbi.nlm.nih.gov/pubmed/31214138
http://dx.doi.org/10.3389/fmicb.2019.01183
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