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. 2006 Dec 15;2(12):e206.
doi: 10.1371/journal.pgen.0020206.

The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia Enterocolitica Strain 8081

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Free PMC article

The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia Enterocolitica Strain 8081

Nicholas R Thomson et al. PLoS Genet. .
Free PMC article

Abstract

The human enteropathogen, Yersinia enterocolitica, is a significant link in the range of Yersinia pathologies extending from mild gastroenteritis to bubonic plague. Comparison at the genomic level is a key step in our understanding of the genetic basis for this pathogenicity spectrum. Here we report the genome of Y. enterocolitica strain 8081 (serotype 0:8; biotype 1B) and extensive microarray data relating to the genetic diversity of the Y. enterocolitica species. Our analysis reveals that the genome of Y. enterocolitica strain 8081 is a patchwork of horizontally acquired genetic loci, including a plasticity zone of 199 kb containing an extraordinarily high density of virulence genes. Microarray analysis has provided insights into species-specific Y. enterocolitica gene functions and the intraspecies differences between the high, low, and nonpathogenic Y. enterocolitica biotypes. Through comparative genome sequence analysis we provide new information on the evolution of the Yersinia. We identify numerous loci that represent ancestral clusters of genes potentially important in enteric survival and pathogenesis, which have been lost or are in the process of being lost, in the other sequenced Yersinia lineages. Our analysis also highlights large metabolic operons in Y. enterocolitica that are absent in the related enteropathogen, Yersinia pseudotuberculosis, indicating major differences in niche and nutrients used within the mammalian gut. These include clusters directing, the production of hydrogenases, tetrathionate respiration, cobalamin synthesis, and propanediol utilisation. Along with ancestral gene clusters, the genome of Y. enterocolitica has revealed species-specific and enteropathogen-specific loci. This has provided important insights into the pathology of this bacterium and, more broadly, into the evolution of the genus. Moreover, wider investigations looking at the patterns of gene loss and gain in the Yersinia have highlighted common themes in the genome evolution of other human enteropathogens.

Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Circular Representation of the Y. enterocolitica Strain 8081 Chromosome
The outer scale shows the size in bps. From the outside in, circles 1 and 2 show the position of CDSs transcribed in a clockwise and anticlockwise direction, respectively (for colour codes see below). Circles 3–5 (all CDSs coloured green) mark the position of Y. enterocolitica strain 8081 genes that have orthologues (by reciprocal FASTA analysis) in Y. pestis strains CO92, 91001, and KIM10+ and in (circle 6) Y. pseudotuberculosis strain IP32953 (CDSs coloured orange), respectively. Circles 7–10 show the Y. enterocolitica strain 8081 CDSs present (as detected by microarray) in all of the Y. enterocolitica isolates tested from biotype 1A (eight strains, red), biotype 2 (two strains, pink), biotype 3 (eight strains, blue), and biotype 4 (eight strains, yellow). Circle 11 shows CDSs unique to Y. enterocolitica strain 8081 (brown) compared with Y. pestis strain CO92 and Y. pseudotuberculosis strain IP32953 as determined by reciprocal FASTA analysis. Circle 12 shows CDSs unique to Y. enterocolitica strain 8081 (black) biotype 1B compared to all isolates of Y. enterocolitica biotypes 1A, 2, 3, and 4 as determined by microarray analysis. Circle 13 shows a plot of G + C content (in a 10-kb window) and circle 14 shows a plot of GC skew ([G − C]/[G + C] in a 10-kb window). Genes in circles 1 and 2 are colour-coded according to the function of their gene products: dark green, membrane or surface structures; yellow, central or intermediary metabolism; cyan, degradation of macromolecules; red, information transfer/cell division; cerise, degradation of small molecules; pale blue, regulators; salmon pink, pathogenicity or adaptation; black, energy metabolism; orange, conserved hypothetical; pale green, unknown; and brown, pseudogenes. The position of prophage elements (pink) and other important regions of difference (mentioned in the text) are marked (red). See Table 2 for a description. LPS, lipopolysaccharide biosynthetic genes.
Figure 2
Figure 2. Distribution of Orthologous CDSs in Y. enterocolitica 8081, Y. pestis CO92, and Y. pseudotuberculosis IP32953
The Venn diagram shows the number of genes unique or shared between two other Yersinia species (see Materials and Methods). The associated pie charts show the breakdown of the functional groups assigned for CDSs in relevant sections of the Venn diagram. Colour code for the pie charts is as follows: hypothetical proteins (1); conserved hypothetical proteins (2); chemotaxis and motility (3); chromosomal replication (4); chaperones (5); protective responses (6); transport and binding proteins (7); adaptations to atypical conditions (8); cell division (9); macromolecule degradation (10); synthesis and modification of macromolecules (11); amino acid biosynthesis (12); biosynthesis of cofactors, prosthetic groups, and carriers (13); central intermediary metabolism (14); small-molecule degradation (15); energy metabolism (16); fatty acid biosynthesis (17); nucleosides and nucleotide biosynthesis and metabolism (18); periplasmic/exported/lipoproteins (19); ribosomal proteins (20); laterally acquired (including prophage CDSs) (21); pathogenicity and virulence (22); general regulation (23); and miscellaneous function (24). Y. en, Y. enterocolitica strain 8081; Y. pstb, Y. pseudotuberculosis strain IP32953; Y. pestis, Y. pestis strain CO92.
Figure 3
Figure 3. Microarray Analysis of the Plasticity Zone of 34 Isolates of Y. enterocolitica Biotypes 1A, 1B, 2, 3, and 4
Microarray analysis of the genomic DNA from 34 Y. enterocolitica isolates, representing five biotypes, constructed using GeneSpring version 6.1 software. Data is presented for the CDS in the range of YE3439–YE3658 including the PZ and YGI-1, as marked (left side). Each numbered column represents the results from a different Y. enterocolitica strain: 1, 09/03; 2, 12/02; 3, 208/02; 4, 35/03; 5, 77/03; 6, 30/02; 7, 81/02; 8, 14/02; 9, 119/02; 10, 212/02; 11, 218/02; 12, 231/02; 13, 56/03; 14, 16/03; 15, 209/02; 16, 149/02; 17, 177/02; 18, 153/02; 19, 202/02; 20, 7/03; 21, 135/02; 22, 8/03; 23, 190/02; 24, 220/02; 25, 227/02; 26, 201/02; 27, Y30; 28, Y73; 29, Y89; 30, Y71; 31, Y68; 32, Y70; 33, Y69; and 34, 8081 (control). See Table S2 for details. The colour-coded biotype key for each isolate is shown at the bottom. Each row represents an individual gene within this region. Coloured blocks (right side) have been used to highlight groups of CDSs showing differing distributions between isolates. The range of CDSs encoded within these blocks is shown (in brackets). Also marked are the relative positions of interesting CDSs or loci that have been mentioned within the body of this article. Blue CDSs correspond to those genes that are considered absent/divergent, and yellow CDSs correspond to genes that are assigned present/conserved. Grey indicates data not obtained.

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