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Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes

BACKGROUND: Fimbriae are bacterial cell surface organelles involved in the pathogenesis of many bacterial species, including Gallibacterium anatis, in which a F17-like fimbriae of the chaperone-usher (CU) family was recently shown to be an important virulence factor and vaccine candidate. To reveal...

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Autores principales: Kudirkienė, Eglė, Bager, Ragnhild J, Johnson, Timothy J, Bojesen, Anders M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299563/
https://www.ncbi.nlm.nih.gov/pubmed/25495603
http://dx.doi.org/10.1186/1471-2164-15-1093
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author Kudirkienė, Eglė
Bager, Ragnhild J
Johnson, Timothy J
Bojesen, Anders M
author_facet Kudirkienė, Eglė
Bager, Ragnhild J
Johnson, Timothy J
Bojesen, Anders M
author_sort Kudirkienė, Eglė
collection PubMed
description BACKGROUND: Fimbriae are bacterial cell surface organelles involved in the pathogenesis of many bacterial species, including Gallibacterium anatis, in which a F17-like fimbriae of the chaperone-usher (CU) family was recently shown to be an important virulence factor and vaccine candidate. To reveal the distribution and variability of CU fimbriae 22 genomes of the avian host-restricted bacteria Gallibacterium spp. were investigated. Fimbrial clusters were classified using phylogeny-based and conserved domain (CD) distribution-based approaches. To characterize the fimbriae in depth evolutionary analysis and in vitro expression of the most prevalent fimbrial clusters was performed. RESULTS: Overall 48 CU fimbriae were identified in the genomes of the examined Gallibacterium isolates. All fimbriae were assigned to γ4 clade of the CU fimbriae of Gram-negative bacteria and were organized in four-gene clusters encoding a putative major fimbrial subunit, a chaperone, an usher and a fimbrial adhesin. Five fimbrial clusters (Flf-Flf4) and eight conserved domain groups were defined to accommodate the identified fimbriae. Although, the number of different fimbrial clusters in individual Gallibacterium genomes was low, there was substantial amino acid sequence variability in the major fimbrial subunit and the adhesin proteins. The distribution of CDs among fimbrial clusters, analysis of their flanking regions, and evolutionary comparison of the strains revealed that Gallibacterium fimbrial clusters likely underwent evolutionary divergence resulting in highly host adapted and antigenically variable fimbriae. In vitro, only the fimbrial subunit FlfA was expressed in most Gallibacterium strains encoding this protein. The absence or scarce expression of the two other common fimbrial subunits (Flf1A and Flf3A) indicates that their expression may require other in vitro or in vivo conditions. CONCLUSIONS: This is the first approach establishing a systematic fimbria classification system within Gallibacterium spp., which indicates a species-wide distribution of γ(4) CU fimbriae among a diverse collection of Gallibacterium isolates. The expression of only one out of up to three fimbriae present in the individual genomes in vitro suggests that fimbriae expression in Gallibacterium is highly regulated. This information is important for future attempts to understand the role of Gallibacterium fimbriae in pathogenesis, and may prove useful for improved control of Gallibacterium infections in chickens. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1093) contains supplementary material, which is available to authorized users.
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spelling pubmed-42995632015-01-21 Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes Kudirkienė, Eglė Bager, Ragnhild J Johnson, Timothy J Bojesen, Anders M BMC Genomics Research Article BACKGROUND: Fimbriae are bacterial cell surface organelles involved in the pathogenesis of many bacterial species, including Gallibacterium anatis, in which a F17-like fimbriae of the chaperone-usher (CU) family was recently shown to be an important virulence factor and vaccine candidate. To reveal the distribution and variability of CU fimbriae 22 genomes of the avian host-restricted bacteria Gallibacterium spp. were investigated. Fimbrial clusters were classified using phylogeny-based and conserved domain (CD) distribution-based approaches. To characterize the fimbriae in depth evolutionary analysis and in vitro expression of the most prevalent fimbrial clusters was performed. RESULTS: Overall 48 CU fimbriae were identified in the genomes of the examined Gallibacterium isolates. All fimbriae were assigned to γ4 clade of the CU fimbriae of Gram-negative bacteria and were organized in four-gene clusters encoding a putative major fimbrial subunit, a chaperone, an usher and a fimbrial adhesin. Five fimbrial clusters (Flf-Flf4) and eight conserved domain groups were defined to accommodate the identified fimbriae. Although, the number of different fimbrial clusters in individual Gallibacterium genomes was low, there was substantial amino acid sequence variability in the major fimbrial subunit and the adhesin proteins. The distribution of CDs among fimbrial clusters, analysis of their flanking regions, and evolutionary comparison of the strains revealed that Gallibacterium fimbrial clusters likely underwent evolutionary divergence resulting in highly host adapted and antigenically variable fimbriae. In vitro, only the fimbrial subunit FlfA was expressed in most Gallibacterium strains encoding this protein. The absence or scarce expression of the two other common fimbrial subunits (Flf1A and Flf3A) indicates that their expression may require other in vitro or in vivo conditions. CONCLUSIONS: This is the first approach establishing a systematic fimbria classification system within Gallibacterium spp., which indicates a species-wide distribution of γ(4) CU fimbriae among a diverse collection of Gallibacterium isolates. The expression of only one out of up to three fimbriae present in the individual genomes in vitro suggests that fimbriae expression in Gallibacterium is highly regulated. This information is important for future attempts to understand the role of Gallibacterium fimbriae in pathogenesis, and may prove useful for improved control of Gallibacterium infections in chickens. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1093) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-12 /pmc/articles/PMC4299563/ /pubmed/25495603 http://dx.doi.org/10.1186/1471-2164-15-1093 Text en © Kudirkienė et al.; licensee BioMed Central. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Kudirkienė, Eglė
Bager, Ragnhild J
Johnson, Timothy J
Bojesen, Anders M
Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title_full Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title_fullStr Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title_full_unstemmed Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title_short Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes
title_sort chaperone-usher fimbriae in a diverse selection of gallibacterium genomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299563/
https://www.ncbi.nlm.nih.gov/pubmed/25495603
http://dx.doi.org/10.1186/1471-2164-15-1093
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