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

ABSTRACT: 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.

SUBMITTER: Flament-Simon SC

PROVIDER: S-EPMC6555128 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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

Flament-Simon Saskia-Camille SC Duprilot Marion M Mayer Noémie N García Vanesa V Alonso María Pilar MP Blanco Jorge J Nicolas-Chanoine Marie-Hélène MH

Frontiers in microbiology 20190531

<h4>Background</h4>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), ...[more]

PMID: 31214138

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Project description:Bacteria form complex multicellular structures on solid surfaces known as biofilms, which allow them to survive in harsh environments. A hallmark characteristic of mature biofilms is the high-level antibiotic tolerance (up to 1,000 times) compared with that of planktonic cells. Here, we report our new findings that biofilm cells are not always more tolerant to antibiotics than planktonic cells in the same culture. Specifically, Escherichia coli RP437 exhibited a dynamic change in antibiotic susceptibility during its early-stage biofilm formation. This phenomenon was not strain specific. Upon initial attachment, surface-associated cells became more sensitive to antibiotics than planktonic cells. By controlling the cell adhesion and cluster size using patterned E. coli biofilms, cells involved in the interaction between cell clusters during microcolony formation were found to be more susceptible to ampicillin than cells within clusters, suggesting a role of cell-cell interactions in biofilm-associated antibiotic tolerance. After this stage, biofilm cells became less susceptible to ampicillin and ofloxacin than planktonic cells. However, when the cells were detached by sonication, both antibiotics were more effective in killing the detached biofilm cells than the planktonic cells. Collectively, these results indicate that biofilm formation involves active cellular activities in adaption to the attached life form and interactions between cell clusters to build the complex structure of a biofilm, which can render these cells more susceptible to antibiotics. These findings shed new light on bacterial antibiotic susceptibility during biofilm formation and can guide the design of better antifouling surfaces, e.g., those with micron-scale topographic structures to interrupt cell-cell interactions.IMPORTANCE Mature biofilms are known for their high-level tolerance to antibiotics; however, antibiotic susceptibility of sessile cells during early-stage biofilm formation is not well understood. In this study, we aim to fill this knowledge gap by following bacterial antibiotic susceptibility during early-stage biofilm formation. We found that the attached cells have a dynamic change in antibiotic susceptibility, and during certain phases, they can be more sensitive to antibiotics than planktonic counterparts in the same culture. Using surface chemistry-controlled patterned biofilm formation, cell-surface and cell-cell interactions were found to affect the antibiotic susceptibility of attached cells. Collectively, these findings provide new insights into biofilm physiology and reveal how adaptation to the attached life form may influence antibiotic susceptibility of bacterial cells.

Project description:BackgroundUropathogenic Escherichia coli (UPEC) is the main etiological agent behind community-acquired and hospital-acquired urinary tract infections (UTIs), which are among the most prevalent human infections. The management of UPEC infections is becoming increasingly difficult owing to multi-drug resistance, biofilm formation, and the possession of an extensive virulence arsenal. This study aims to characterize UPEC isolates in Tanta, Egypt, with regard to their antimicrobial resistance, phylogenetic profile, biofilm formation, and virulence, as well as the potential associations among these factors.MethodsOne hundred UPEC isolates were obtained from UTI patients in Tanta, Egypt. Antimicrobial susceptibility was assessed using the Kirby-Bauer method. Extended-spectrum β-lactamases (ESBLs) production was screened using the double disk synergy test and confirmed with PCR. Biofilm formation was evaluated using the microtiter-plate assay and microscopy-based techniques. The phylogenetic groups of the isolates were determined. The hemolytic activity, motility, siderophore production, and serum resistance of the isolates were also evaluated. The clonal relatedness of the isolates was assessed using ERIC-PCR.ResultsIsolates displayed elevated resistance to cephalosporins (90-43%), sulfamethoxazole-trimethoprim (63%), and ciprofloxacin (53%). Ninety percent of the isolates were multidrug-resistant (MDR)/ extensively drug-resistant (XDR) and 67% produced ESBLs. Notably, there was an inverse correlation between biofilm formation and antimicrobial resistance, and 31%, 29%, 32%, and 8% of the isolates were strong, moderate, weak, and non-biofilm producers, respectively. Beta-hemolysis, motility, siderophore production, and serum resistance were detected in 64%, 84%, 65%, and 11% of the isolates, respectively. Siderophore production was correlated to resistance to multiple antibiotics, while hemolysis was more prevalent in susceptible isolates and associated with stronger biofilms. Phylogroups B2 and D predominated, with lower resistance and stronger biofilms in group B2. ERIC-PCR revealed considerable diversity among the isolates.ConclusionThis research highlights the dissemination of resistance in UPEC in Tanta, Egypt. The evident correlation between biofilm and resistance suggests a resistance cost on bacterial cells; and that isolates with lower resistance may rely on biofilms to enhance their survival. This emphasizes the importance of considering biofilm formation ability during the treatment of UPEC infections to avoid therapeutic failure and/or infection recurrence.

Dataset Information

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

Publications

Association Between Kinetics of Early Biofilm Formation and Clonal Lineage in <i>Escherichia coli</i>.

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