Genome rearrangements and phylogeny reconstruction in Yersinia pestis

Abstract

Genome rearrangements have played an important role in the evolution of Yersinia pestis from its progenitor Yersinia pseudotuberculosis. Traditional phylogenetic trees for Y. pestis based on sequence comparison have short internal branches and low bootstrap supports as only a small number of nucleotide substitutions have occurred. On the other hand, even a small number of genome rearrangements may resolve topological ambiguities in a phylogenetic tree. We reconstructed phylogenetic trees based on genome rearrangements using several popular approaches such as Maximum likelihood for Gene Order and the Bayesian model of genome rearrangements by inversions. We also reconciled phylogenetic trees for each of the three CRISPR loci to obtain an integrated scenario of the CRISPR cassette evolution. Analysis of contradictions between the obtained evolutionary trees yielded numerous parallel inversions and gain/loss events. Our data indicate that an integrated analysis of sequence-based and inversion-based trees enhances the resolution of phylogenetic reconstruction. In contrast, reconstructions of strain relationships based on solely CRISPR loci may not be reliable, as the history is obscured by large deletions, obliterating the order of spacer gains. Similarly, numerous parallel gene losses preclude reconstruction of phylogeny based on gene content.

Keywords: Bacteria evolution; Genome rearrangements; Phylogeny reconstruction.

Figure 1. (A) Phylogenetic tree of the Yersinia spp., based on nucleotide alignments of 2408 single-copy universal genes; (B) phylogenetic tree of the Y. pestis branch only.

Figure 2. Phylogenetic trees network of the Yersinia pestis with Bayesian posterior probability threshold = 0.1.

Figure 3. Phylogenetic trees of the Yersinia spp. based on gene order.

(A) Optimal topology based on inversions. (B) Optimal topology based on all types of rearrangements. Nodes that produce differences in the trees are labeled in red.

Figure 4. CRISPR cassettes of completely sequenced Y. pestis strains. Cassette IDs and spacer numbers are given according to CRISPRdb (Grissa, Vergnaud & Pourcel, 2007).

Identical spacers are shown by the same color; unique spacers are set in frames.

Figure 5. Cladograms (A, B, C) and schemas of evolution (D, E, F) of three CRISPR loci of Y. pestis. (A, D) The main, most variable, locus; (B, E) additional locus 1; (C, D) additional locus 2.

Figure 6. Cladograms (A, B) and schemas of evolution (C, D) of two integrated CRISPR-based maximum parsimony phylogenetic trees most compatible with the sequence tree.