Review
doi: 10.1128/MMBR.00014-07.Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek
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- PMID:18063717
- PMCID: PMC2168650
- DOI: 10.1128/MMBR.00014-07
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Review
Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek
Sean-Paul Nuccio et al. Microbiol Mol Biol Rev.2007 Dec.
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Abstract
Many Proteobacteria use the chaperone/usher pathway to assemble proteinaceous filaments on the bacterial surface. These filaments can curl into fimbrial or nonfimbrial surface structures (e.g., a capsule or spore coat). This article reviews the phylogeny of operons belonging to the chaperone/usher assembly class to explore the utility of establishing a scheme for subdividing them into clades of phylogenetically related gene clusters. Based on usher amino acid sequence comparisons, our analysis shows that the chaperone/usher assembly class is subdivided into six major phylogenetic clades, which we have termed alpha-, beta-, gamma-, kappa-, pi-, and sigma-fimbriae. Members of each clade share related operon structures and encode fimbrial subunits with similar protein domains. The proposed classification system offers a simple and convenient method for assigning newly discovered chaperone/usher systems to one of the six major phylogenetic groups.
Figures
Schematic drawing of fimbrial assembly by the chaperone/usher pathway. The N-terminal signal peptide of fimbrial subunits is cleaved during their transport across the cytoplasmic membrane (CM) by the general secretory pathway (Sec). In the periplasm (PP), the chaperone (C) completes the Ig-like fold of fimbrial subunits with its donor β-strand (black arrow). Interaction of the chaperone/fimbrial subunit complexes with the usher protein (U) facilitates the replacement of the chaperone donor β-strand with the N-terminal β-strand of a second subunit, thereby joining subunits into a filament that is transported across the outer membrane (OM). Filaments may curl into helical structures with two subunits per turn (thin, flexible fibrillae), as shown in this schematic drawing. Alternatively, subunits may assemble helices with 3 to 3.4 subunits per turn (thick, rigid fimbriae) or coil up into nonfimbrial, capsule-like structures on the cell surface. In some cases, fimbrial filaments carry a tip adhesin at their distal end, which mediates attachment.
Phylogenetic tree of the FUP family. The graph shows an unrooted phenogram generated using usher amino acid sequences listed in Table S1 in the supplemental material. Ushers are grouped into six fimbrial clades (highlighted in gray) termed α, β, γ, κ, π, and σ. Bootstrap values of nodes defining these clades (indicated by open circles at the base of each fimbrial clade) are shown. The phylogenetic tree and bootstrap values were generated as follows. Usher amino acid sequences were aligned using ClustalW (MacVector 7.2.3) with a BLOSUM 30 matrix for pairwise alignment and a BLOSUM series matrix for multiple alignment, both with default settings. The phylogeny inference package software (PHYLIP 3.65) developed by Felsenstein (93) was used to perform the remaining analyses. Bootstrapping of the aligned usher sequences was performed in triplicate using the bootstrap algorithm of BOOTSTRAP to determine the number of instances, out of 1,000 sets analyzed (using random seeds 123, 345, and 567), where the members of each clade grouped completely behind the displayed node. Protein distance matrices were generated with PROTDIST using a Jones-Taylor-Thornton matrix with default settings for the unrooted tree or set to analyze 1,000 data sets for bootstrapping. Neighbor joining was performed with NEIGHBOR with default settings or set to analyze 1,000 data sets using the random seeds 345, 567, and 789, respectively, for the above-mentioned bootstrapping runs. Consensus trees (not shown) to interpret the bootstrap data were generated using the majority-rule-extended algorithm of CONSENSE. The unrooted phenogram displayed was generated using DRAWTREE without tree improvement iteration.
Phylogenetic relationship of operons belonging to the α-fimbriae. The branch of the FUP tree representing α-fimbriae is shown on the left. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. IS, homology to insertion sequence (IS) element.
Phylogenetic relationship of operons belonging to the β-fimbriae. (A) The branch of the FUP tree representing β-fimbriae is shown on the left. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. IS, homology to IS element. (B) Comparison of thegltB-yhcG intergenic regions inE. coli strain K-12 andS. enterica serotype Typhimurium strain LT2. Genes are indicated by arrows.
Phylogenetic relationship of operons belonging to the γ1-, γ2-, and γ3-fimbriae. The branch of the FUP tree representing γ1-, γ2-, and γ3-fimbriae is shown on the left. The bootstrap value for the node defining each subclade is displayed at the top and was generated in the analysis performed for Fig. 2. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. IS, homology to IS element;in, homology to invasin domain PFAM05775; rt, homology to reverse transcriptase; ds, homology to DsbA.
Phylogenetic relationship of operons belonging to the γ4-fimbriae. The branch of the FUP tree representing γ4-fimbriae is shown on the left. The bootstrap value for the node defining the γ4-fimbriae is displayed at the top and was generated in the analysis performed for Fig. 2. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom.
Phylogenetic relationship of operons belonging to the κ-fimbriae. The branch of the FUP tree representing κ-fimbriae is shown on the left. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom.
Phylogenetic relationship of operons belonging to the π-fimbriae. The branch of the FUP tree representing π-fimbriae is shown on the left. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. NG, not grouped but related to π-fimbriae; IS, homology to IS element.
Phylogenetic relationship of operons belonging to the σ-fimbriae. The branch of the FUP tree representing σ-fimbriae is shown on the left. Numbers at the end of each branch of the phylogenetic tree correspond to the numbers given for each operon in the center. The gene order for each operon is shown on the right (arrows). The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. fk, homology to flagellum hook-associated protein; SCPU, spore coat protein U.
Evolution of fimbrial operons of the chaperone/usher assembly class from a hypothetical ancestor. The predicted functions for each gene product and the sequence homologies to protein families are indicated in the legend at the bottom. For a detailed discussion, see the text.
Phylogenetic tree of fimbrial chaperones. An unrooted phenogram illustrating the phylogenetic relatedness of the chaperones associated with the ushers listed in Table S1 in the supplemental material is shown. Chaperone amino acid sequences were aligned and analyzed in the same fashion as that described in the legend of Fig. 2. Although PapJ has been shown to act in some capacity as a periplasmic chaperone (326), it and its homologues (PixJ, SfpJ, and PrfJ) were not included in this analysis, as they do not possess a fimbrial chaperone domain, nor do they share sequence similarity with other fimbrial proteins. The six fimbrial clades (α, β, γ, κ, π, and σ) defined by sequence comparison of usher proteins (Fig. 2) are indicated in the phenogram using gray highlighting. Arrows and circled branches indicate operons containing multiple chaperone genes and are inserted to the right and below the phenogram. The positions of chaperone genes in fimbrial operons (open arrows) in the phenogram are indicated by lowercase letters or by black arrows.
References
- Abe, N., K. Moriishi, M. Saito, and M. Naiki. 1993. Confirmed nucleotide sequence of fanF of Escherichia coli K99 fimbriae. Jpn. J. Vet. Res. 41:97-99. - PubMed
- Adams, L. M., C. P. Simmons, L. Rezmann, R. A. Strugnell, and R. M. Robins-Browne. 1997. Identification and characterization of a K88- and CS31A-like operon of a rabbit enteropathogenic Escherichia coli strain which encodes fimbriae involved in the colonization of rabbit intestine. Infect. Immun. 65:5222-5230. - PMC - PubMed
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