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Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes.

ABSTRACT: 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 ?4 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 ?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.

SUBMITTER: Kudirkiene E

PROVIDER: S-EPMC4299563 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes.

Kudirkienė Eglė E Bager Ragnhild J RJ Johnson Timothy J TJ Bojesen Anders M AM

BMC genomics 20141212

<h4>Background</h4>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 a ...[more]

PMID: 25495603

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Project description:Salmonella is one of the most successful foodborne pathogens worldwide, owing in part to its ability to colonize or infect a wide range of hosts. Salmonella serovars are known to encode a variety of different fimbriae (hairlike organelles that facilitate binding to surfaces); however, the distribution, number, and sequence diversity of fimbriae encoded across different lineages of Salmonella were unknown. We queried whole-genome sequence (WGS) data for 242 Salmonella enterica subsp. enterica (subspecies enterica) isolates from the top 217 serovars associated with isolation from humans and agricultural animals; this effort identified 2,894 chaperone-usher (CU)-type fimbrial usher sequences, representing the most conserved component of CU fimbriae. On average, isolates encoded 12 different CU fimbrial ushers (6 to 18 per genome), although the distribution varied significantly (P = 1.328E-08) by phylogenetic clade, with isolates in section Typhi having significantly fewer fimbrial ushers than isolates in clade A2 (medians = 10 and 12 ushers, respectively). Characterization of fimbriae in additional non-enterica subspecies genomes suggested that 8 fimbrial ushers were classified as being unique to subspecies enterica isolates, suggesting that the majority of fimbriae were most likely acquired prior to the divergence of subspecies enterica. Characterization of mobile elements suggested that plasmids represent an important vehicle facilitating the acquisition of a wide range of fimbrial ushers, particularly for the acquisition of fimbriae from other Gram-negative genera. Overall, our results suggest that differences in the number and type of fimbriae encoded most likely reflect differences in phylogenetic clade rather than differences in host range. IMPORTANCE Fimbriae of the CU assembly pathway represent important organelles that mediate Salmonella's interactions with host tissues and abiotic surfaces. Our analyses provide a comprehensive overview of the diversity of CU fimbriae in Salmonella spp., highlighting that the majority of CU fimbriae are distributed broadly across multiple subspecies and suggesting that acquisition most likely occurred prior to the divergence of subspecies enterica. Our data also suggest that plasmids represent the primary vehicles facilitating the horizontal transfer of diverse CU fimbriae in Salmonella. Finally, the observed high sequence similarity between some ushers suggests that different names may have been assigned to closely related fimbrial ushers that likely should be represented by a single designation. This highlights the need to establish standard criteria for fimbria classification and nomenclature, which will also facilitate future studies seeking to associate virulence factors with adaptation to or differences in the likelihood of causing disease in a given host.

Dataset Information

Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes.

Publications

Chaperone-usher fimbriae in a diverse selection of Gallibacterium genomes.

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