Complete genome sequence of a Yersinia enterocolitica "Old World" (3/O:9) strain and comparison with the "New World" (1B/O:8) strain

Abstract

Yersinia enterocolitica is a heterogeneous bacterial species with a wide range of animal reservoirs through which human intestinal illness can be facilitated. In contrast to the epidemiological pattern observed in the United States, infections in China present a pattern similar to those in European countries and Japan, wherein "Old World" strains (biotypes 2 to 5) are prevalent. To gain insights into the evolution of Y. enterocolitica and pathogenic properties toward human hosts, we sequenced the genome of a biotype 3 strain, 105.5R(r) (O:9), obtained from a Chinese patient. Comparative genome sequence analysis with strain 8081 (1B/O:8) revealed new insights into Y. enterocolitica. Both strains have more than 14% specific genes. In strain 105.5R(r), putative virulence factors were found in strain-specific genomic pathogenicity islands that comprised a novel type III secretion system and rtx-like genes. Many of the loci representing ancestral clusters, which are believed to contribute to enteric survival and pathogenesis, are present in strain 105.5R(r) but lost in strain 8081. Insertion elements in 105.5R(r) have a pattern distinct from those in strain 8081 and were exclusively located in a strain-specific region. In summary, our comparative genome analysis indicates that these two strains may have attained their pathogenicity by completely separate evolutionary events, and the 105.5R(r) strain, a representative of the Old World biogroup, lies in a branch of Y. enterocolitica that is distinct from the "New World" 8081 strain.

Fig. 1.

Circular representation of the strain 105.5R(r) chromosome. The outer scale shows the size in bp. From the outside in, the first circle shows strain 105.5R(r)-specific genomic islands, compared with those for 8081; the second and third circles show the positions of CDSs transcribed in clockwise and counterclockwise directions, respectively; the fourth circle shows rRNA and tRNA; the fifth circle shows the IS elements; and the sixth circle shows a plot of GC skew ([G-C]/[G+C] in a 10-kb window). LPS, lipopolysaccharide.

Fig. 2.

Whole-genome comparison of strains 105.5R(r) and 8081. The coordinate image shows the whole-genome sequence alignment (per the MUMmer package, version 3.0). The forward and reverse matches are indicated by the upward and downward slopes, respectively. The line graph set above shows the locations of indels, including specific genes and genomic islands, in strain 105.5R(r).

Fig. 3.

Comparison of gene contents in strains 105.5R(r) and 8081. (A) Venn diagram of the orthologous and specific genes in each strain. (B) COG categories of the orthologous and specific genes in each strain. The alphabetic code for the column charts is as follows: C, energy production and conversion; D, cell division and chromosome partitioning; E, amino acid transport and metabolism; F, nucleotide transport and metabolism; G, carbohydrate transport and metabolism; H, coenzyme metabolism; I, lipid metabolism; J, translation, ribosomal structure, and biogenesis; K, transcription; L, DNA replication, recombination, and repair; M, cell envelope biogenesis, outer membrane; N, cell motility and secretion; O, posttranslational modification, protein turnover, and chaperones; P, inorganic ion transport and metabolism; Q, secondary metabolite biosynthesis, transport, and catabolism; R, general function prediction only; S, function unknown; T, signal transduction mechanisms; U, intracellular trafficking, secretion, and vesicular transport; V, defense mechanisms.

Fig. 4.

Cladogram based on the amino acid sequence data of type III secretion systems. The phylogenetic analysis was based on the sequences of 51 T3SSs within 17 genera and performed with the neighbor-joining method. Calculations were performed using the two-parameter model.

Fig. 5.

Comparison of the aat clusters in strain 105.5R(r) and Escherichia coli strain 042(EAEC). The aat gene cluster is known to encode a specialized ABC transporter, which promotes pathogenesis by transporting virulent effector proteins out of the bacterial cell. aggR encodes the transcriptional activator of the aat gene cluster. Genes are distinguished by grayscale, and the corresponding size scale is drawn below.