Bordetella species are distinguished by patterns of substantial gene loss and host adaptation - PubMed (original) (raw)

Comparative Study

Bordetella species are distinguished by patterns of substantial gene loss and host adaptation

C A Cummings et al. J Bacteriol. 2004 Mar.

Abstract

Pathogens of the bacterial genus Bordetella cause respiratory disease in humans and animals. Although virulence and host specificity vary across the genus, the genetic determinants of this diversity remain unidentified. To identify genes that may underlie key phenotypic differences between these species and clarify their evolutionary relationships, we performed a comparative analysis of genome content in 42 Bordetella strains by hybridization of genomic DNA to a microarray representing the genomes of three Bordetella species and by subtractive hybridization. Here we show that B. pertussis and B. parapertussis are predominantly differentiated from B. bronchiseptica by large, species-specific regions of difference, many of which encode or direct synthesis of surface structures, including lipopolysaccharide O antigen, which may be important determinants of host specificity. The species also exhibit sequence diversity at a number of surface protein-encoding loci, including the fimbrial major subunit gene, fim2. Gene loss, rather than gene acquisition, accompanied by the proliferation of transposons, has played a fundamental role in the evolution of the pathogenic bordetellae and may represent a conserved evolutionary mechanism among other groups of microbial pathogens.

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Figures

FIG.1.

FIG.1.

CGH of 42 Bordetella strains. Each column represents a strain, ordered and color-coded according to the tree topology shown in Fig. 2. The three sequenced strains are marked by asterisks. B. pertussis strain 18323 is indicated by the dagger. Each row represents a microarray probe, arranged in RB50 gene order from “start” to “end,” with RB50 genome coordinates listed on the left. φ indicates clusters of phage genes. Arrowheads indicate regions of >5 kb not represented by a probe. Magenta bar, duplicated sequences in RB50. The chromosomal locations of the largest of these duplications, a degenerate prophage, are marked by magenta arrowheads. Yellow bar, genes not present in the RB50 sequence, arranged in Tohama I gene order. The values below the color bar at the bottom refer to log2(test/reference intensities). Missing data are gray. Bp, B. pertussis; Bb, B. bronchiseptica; Bpp, B. parapertussis.

FIG. 2.

FIG. 2.

Phylogeny of Bordetella strains based on CGH data. Phylogenetic associations were inferred using a maximum-parsimony algorithm, and confidence intervals were determined from 100 bootstrapped datasets. The scale bar represents 100 evolutionary events (steps), and bootstrap values of ≥50% are indicated (19). The presence of Bordetella IS elements, as detected by CGH, is indicated for each strain: blue boxes, IS_481_; yellow, IS_1002_; and green, IS1663. The presence of IS_1001_ (magenta), which was not represented on the array, is taken from reference . In that study, the presence of IS_1001_ was not determined for B. pertussis, excepting strains Tohama I and 18323. In parentheses following each strain number are the strain's host and alias. Sequenced strains are shaded. The diamond indicates the B. bronchiseptica clade that may be associated with B. pertussis. The inset shows an overview tree of an equally likely phylogeny, created by collapsing all branches supported by bootstrap values of ≥50.

FIG. 3.

FIG. 3.

Gene content variation and structural differences in the LPS O-antigen biosynthesis region. CGH data for the O-antigen biosynthesis region in 42 Bordetella strains are shown, displayed as in Fig. 1, with strain groups color coded according to the tree topology shown in Fig. 2. Some ORFs are represented by multiple probes. Coding sequence designations, gene names, and annotations are included. The color scale is as in Fig. 1.

FIG. 4.

FIG. 4.

Gene content variation and sequence polymorphism in fimbriae genes. Strain groups are color coded according to the tree topology shown in Fig. 2. For each probe, the sequenced strain from which it was amplified is listed, as well as the percent sequence identity of the probe to each of the three sequenced genomes. The color scale and symbols are as in Fig. 1.

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