Lateral gene transfer, rearrangement, reconciliation

Abstract

Background: Models of ancestral gene order reconstruction have progressively integrated different evolutionary patterns and processes such as unequal gene content, gene duplications, and implicitly sequence evolution via reconciled gene trees. These models have so far ignored lateral gene transfer, even though in unicellular organisms it can have an important confounding effect, and can be a rich source of information on the function of genes through the detection of transfers of clusters of genes.

Result: We report an algorithm together with its implementation, DeCoLT, that reconstructs ancestral genome organization based on reconciled gene trees which summarize information on sequence evolution, gene origination, duplication, loss, and lateral transfer. DeCoLT optimizes in polynomial time on the number of rearrangements, computed as the number of gains and breakages of adjacencies between pairs of genes. We apply DeCoLT to 1099 gene families from 36 cyanobacteria genomes.

Conclusion: DeCoLT is able to reconstruct adjacencies in 35 ancestral bacterial genomes with a thousand gene families in a few hours, and detects clusters of co-transferred genes. DeCoLT may also be used with any relationship between genes instead of adjacencies, to reconstruct ancestral interactions, functions or complexes.

Availability: http://pbil.univ-lyon1.fr/software/DeCoLT/

Figure 1

Adjacency evolution. The evolution of an adjacency within a dated species tree, along reconciled gene phylogenies. The gene trees are blue and purple, while red horizontal edges are adjacencies. The time slices t₀, ..., t₃ indicate in which order the speciation nodes (big green nodes) occur, and are used to localize genes in the species tree (a branch and a time slice give the coordinates of a gene or an event). Red crosses mean gene losses, for example in the branches leading to A or C (adjacencies are lost when one extremity is lost), or an adjacency breakage, for example in the branch leading to D (gene loss and adjacency breakages are different events, since a gene loss is not a rearrangement while a breakage is, and only rearrangements are counted in the objective function). Here one adjacency is gained in the branch leading to species C, one is broken in the branch leading to species D, and one is transferred from the branch leading to B to the branch leading to C. The transfer implies first a speciation outside the species phylogeny, and then a transfer which can be in another time slice. A tandem duplication in the branch leading to A gives a new adjacency between the two copies.

Figure 2

Propagation rules. Propagation rules for an adjacency ab: a function of the events happening to its extremities a and b (events happening to a are written on the left, events happening to b are written on the right). If a₁, a₂, b₁ and b₂ are the children of a and b. Numbers on each subsquare are recurrence rules following the propagation rule. Recurrence rules add the possibility of rearrangements at each step. For combination of duplication or loss with another event not mentioned here, follow the rule with "no event" (the duplication or loss is supposed to happen first).

Figure 3

Cyanobacteria phylogeny. Cyanobacteria dated species tree. The size (area) and colours of internal nodes is the ratio of the number of adjacencies over the number of genes in every ancestral species.

Figure 4

Circularity of ancestral genomes. On the x axis is the degree of a gene, that is, the number of adjacencies it belongs to, and on the y axis there is the proportion of genes with this degree. In black, there are the values for the sequence trees and in red for ALE trees.