The fate of laterally transferred genes: life in the fast lane to adaptation or death

Abstract

Large-scale genome arrangement plays an important role in bacterial genome evolution. A substantial number of genes can be inserted into, deleted from, or rearranged within genomes during evolution. Detecting or inferring gene insertions/deletions is of interest because such information provides insights into bacterial genome evolution and speciation. However, efficient inference of genome events is difficult because genome comparisons alone do not generally supply enough information to distinguish insertions, deletions, and other rearrangements. In this study, homologous genes from the complete genomes of 13 closely related bacteria were examined. The presence or absence of genes from each genome was cataloged, and a maximum likelihood method was used to infer insertion/deletion rates according to the phylogenetic history of the taxa. It was found that whole gene insertions/deletions in genomes occur at rates comparable to or greater than the rate of nucleotide substitution and that higher insertion/deletion rates are often inferred to be present at the tips of the phylogeny with lower rates on more ancient interior branches. Recently transferred genes are under faster and relaxed evolution compared with more ancient genes. Together, this implies that many of the lineage-specific insertions are lost quickly during evolution and that perhaps a few of the genes inserted by lateral transfer are niche specific.

Figure 1.

Bayesian tree obtained for the concatenated sequence of gmk, glpF, and pycA genes. The abbreviations are (Ba₁) Bacillus anthracis Ames; (Ba₂) Bacillus anthracis “Ames Ancestor”; (Ba₃) Bacillus anthracis Sterne; (Bt) Bacillus thuringiensis; (Bc₁) Bacillus cereus ZK; (Bc₂) Bacillus cereus ATCC 10,987; (Bc₃) Bacillus cereus ATCC 14,579; (Gk) Geobacillus kaustophilus; (Bl) Bacillus licheniformis; (Bs) Bacillus subtilis; (Bk) Bacillus clausii; (Bh) Bacillus halodurans; and (Oi) Oceanobacillus iheyensis.

Figure 2.

Different insertion/deletion rates were assumed on the phylogeny. The rate on the branches of the Bc group is α (boxed), the rate on the branch leading to the Bc group is γ (in black), the rate on the remaining branches is β (hatched). Case 1: a single constant rate throughout the phylogeny (α = β = γ). Case 2: two rates differentiate the Bc group (α, β = γ). Case 3: three rates differentiate the Bc group and the branch leading to this group (α, β, γ).

Figure 3.

An example of the likelihood surface with different rates of insertion and deletion. The likelihood value shows a continuous pattern of change as the insertion/deletion rate changes.

Figure 4.

Rapid evolution in the Bc group specific genes. (A) Tree length for the Bc taxa as indicated by genes that are present only within this group of taxa; (B) tree length for the Bc taxa as indicated by genes that are present in all 13 strains.

Figure 5.

K_a/K_s ratio of different group-specific genes. Data are measured using the genes present in the Bc group (Ba₁, Bt, and Bc₁). (A) Genes present in the Bc group; (B) Genes present in Bc, Gk, Bl, and Bs; (C) genes present in Bc, Gk, Bl, Bs, Bk, and Bh; (D) genes present in all 13 strains.