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Biofilm forming properties of quinolone resistant Escherichia coli from the broiler production chain and their dynamics in mixed biofilms.

ABSTRACT: BACKGROUND:Quinolone resistant Escherichia coli (QREC) have been found in samples from Norwegian broiler chicken, despite quinolones not being administered to poultry in Norway. Biofilm production may be one factor contributing to the observed persistence in the broiler production chain. In the present study, 158 QREC strains from chicken caecal and retail meat samples were screened for biofilm production in microtiter plates, biofilm morphotype on Congo Red (CR) agar plates and phylotype by multiplex PCR. Furthermore, the dynamics in mixed biofilms with strains of different morphotypes were studied on glass slides and on CR agar plates. RESULTS:All strains but one produced biofilm in microtiter plates and/or on CR agar plates at room temperature. There were no differences between strains from chicken caecum and chicken retail meat in the mean amount of biofilm produced in microtiter plates. Furthermore, no differences in biofilm production were observed between phylotypes. However, significant differences in biofilm production were found between biofilm morphotypes. The morphotype RDAR (red dry and rough, which has both curli and cellulose in the matrix, was displayed by 70% of the strains. Mean biofilm production by these strains were significantly higher than by strains with the morphotypes PDAR (pink dry and rough) with only cellulose or BDAR (brown dry and rough) with only curli. Interestingly, the two latter morphotypes produced biofilms with the morphotype RDAR when grown together. None of the strains achieved significantly higher numbers of colony forming units (cfu) in mixed biofilms than in single strain biofilms on glass slides. CONCLUSIONS:The results indicate that QREC can form biofilm reservoirs on both inert and organic surfaces in production environments, as well as on meat. This may contribute to persistence and dissemination of the strains. Strains with both curli and cellulose in the biofilm matrix were significantly better biofilm formers than strains lacking one of these components. However, strains with only one of the components could compensate for this by producing mixed biofilms with strains having the other component, and thereby most likely enhance their probabilities of persistence in the production environment.

SUBMITTER: Nesse LL

PROVIDER: S-EPMC7055085 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Biofilm forming properties of quinolone resistant Escherichia coli from the broiler production chain and their dynamics in mixed biofilms.

Nesse Live L LL Osland Ane Mohr AM Mo Solveig S SS Sekse Camilla C Slettemeås Jannice S JS Bruvoll Anna Eline E AEE Urdahl Anne Margrete AM Vestby Lene K LK

BMC microbiology 20200304 1

<h4>Background</h4>Quinolone resistant Escherichia coli (QREC) have been found in samples from Norwegian broiler chicken, despite quinolones not being administered to poultry in Norway. Biofilm production may be one factor contributing to the observed persistence in the broiler production chain. In the present study, 158 QREC strains from chicken caecal and retail meat samples were screened for biofilm production in microtiter plates, biofilm morphotype on Congo Red (CR) agar plates and phylotyp ...[more]

PMID: 32131730

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Project description:In Norway, the use of quinolones in livestock populations is very low, and prophylactic use is prohibited. Despite this, quinolone-resistant Escherichia coli (QREC) isolates are present at low levels in several animal species. The source of these QREC isolates is unknown. The aim of this study was to characterize and compare QREC isolates from different animal species to identify putative factors that may promote the occurrence of QREC. A total of 280 QREC isolates, from broilers, pigs, red foxes, and wild birds, were whole-genome sequenced and analyzed. Well-known chromosomal and plasmid-mediated resistance mechanisms were identified. In addition, mutations in marR, marA, and rpoB causing novel amino acid substitutions in their respective proteins were detected. Phylogenetic analyses were used to determine the relationships between the isolates. Quinolone resistance mechanism patterns appeared to follow sequence type groups. Similar QREC isolates with similar resistance mechanism patterns were detected from the samples, and further phylogenetic analysis indicated close evolutionary relationships between specific isolates from different sources. This suggests the dissemination of highly similar QREC isolates between animal species and also the persistence of QREC strains within the broiler production chain. This highlights the importance of both control measures at the top of the production chain as well as biosecurity measures to avoid the further dissemination and persistence of QREC in these environments.IMPORTANCE Since antimicrobial usage is low in Norwegian animal husbandry, Norway is an ideal country to study antimicrobial resistance in the absence of selective pressure from antimicrobial usage. In particular, the usage of quinolones is very low, which makes it possible to investigate the spread and development of quinolone resistance in natural environments. Comparison of quinolone-resistant E. coli (QREC) isolates from livestock and wild animals in light of this low quinolone usage provides new insights into the development and dissemination of QREC in both natural and production environments. With this information, preventive measures may be taken to prevent further dissemination within Norwegian livestock and between other animals, thus maintaining the favorable situation in Norway.

Project description:Enteroinvasive Escherichia coli (EIEC) is a diarrheagenic E. coli pathotype carrying a virulence plasmid that encodes a type III secretion system (TTSS) directly implicated in bacterial cell invasion. Since 2012, EIEC serotype O96:H19 has been recognized in Europe, Colombia, and most recently Uruguay. In addition to the invasion phenotype, the strains isolated from Colombian children with moderate-to-severe gastroenteritis had a strong biofilm formation phenotype, and as a result, they are referred to as biofilm-forming enteroinvasive E. coli (BF-EIEC). The objective of this study was to characterize the biofilm formation phenotype of the BF-EIEC O96:H19 strain 52.1 isolated from a child with moderate-to-severe gastroenteritis in Colombia. Random mutagenesis using Tn5 transposons identified 100 mutants unable to form biofilm; 20 of those had mutations within the pgaABCD operon. Site-directed mutagenesis of pgaB and pgaC confirmed the importance of these genes in N-acetylglucosamine-mediated biofilm formation. Both biofilm formation and TTSS-mediated host cell invasion were associated with host cell damage on the basis of cytotoxic assays comparing the wild type, invasion gene mutants, and biofilm formation mutants. Multilocus sequence typing-based phylogenetic analysis showed that BF-EIEC strain 52.1 does not cluster with classic EIEC serotype strains. Instead, BF-EIEC strain 52.1 clusters with EIEC serotype O96:H19 strains described in Europe and Uruguay. In conclusion, BF-EIEC O96:H19, an emerging pathogen associated with moderate-to-severe acute gastroenteritis in children under 5 years of age in Colombia, invades cells and has a strong biofilm formation capability. Both phenotypes are independently associated with in vitro cell cytotoxicity, and they may explain, at least in part, the higher disease severity reported in Europe and Latin America. IMPORTANCE Enteroinvasive Escherichia coli (EIEC), a close relative of Shigella, is implicated in dysenteric diarrhea. EIEC pathogenicity involves cell invasion mediated by effector proteins delivered by a type III secretion system (TTSS) that disrupt the cell cytoskeleton. These proteins and the VirF global regulator are encoded by a large (>200 kb) invasion plasmid (pINV). This study reports an emergent EIEC possessing a cell invasion phenotype and a strong polysaccharide matrix-mediated biofilm formation phenotype. Both phenotypes contribute to host cell cytotoxicity in vitro and may contribute to the severe disease reported among children and adults in Europe and Latin America.

Dataset Information

Biofilm forming properties of quinolone resistant Escherichia coli from the broiler production chain and their dynamics in mixed biofilms.

Publications

Biofilm forming properties of quinolone resistant Escherichia coli from the broiler production chain and their dynamics in mixed biofilms.

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