Horizontal gene transfer among genomes: the complexity hypothesis

Abstract

Increasingly, studies of genes and genomes are indicating that considerable horizontal transfer has occurred between prokaryotes. Extensive horizontal transfer has occurred for operational genes (those involved in housekeeping), whereas informational genes (those involved in transcription, translation, and related processes) are seldomly horizontally transferred. Through phylogenetic analysis of six complete prokaryotic genomes and the identification of 312 sets of orthologous genes present in all six genomes, we tested two theories describing the temporal flow of horizontal transfer. We show that operational genes have been horizontally transferred continuously since the divergence of the prokaryotes, rather than having been exchanged in one, or a few, massive events that occurred early in the evolution of prokaryotes. In agreement with earlier studies, we found that differences in rates of evolution between operational and informational genes are minimal, suggesting that factors other than rate of evolution are responsible for the observed differences in horizontal transfer. We propose that a major factor in the more frequent horizontal transfer of operational genes is that informational genes are typically members of large, complex systems, whereas operational genes are not, thereby making horizontal transfer of informational gene products less probable (the complexity hypothesis).

Figure 1

A comparison of the early and the continual horizontal transfer hypotheses. In the continual hypothesis (A), the horizontal arrows indicate that the transfer of operational genes has been occurring since the last common ancestor of prokaryotes. In the early massive hypothesis (B), the single large arrow indicates that one or a few massive horizontal transfer events preceded the diversification of the eubacteria.

Figure 2

Paralog rooting of the operational and informational trees. Roots of trees calculated from operational (A) and informational (B) genes are shown. A one-letter code indicates that the paralog root is found in a terminal branch of the tree, as follows: a, Aquifex; b, Bacillus; c, Synechocystis; e, Escherichia; f, Archaeoglobus; and m, Methanococcus. A double-letter code indicates that the paralog root is found in the internal branch that defines a clade as follows: eb, Escherichia–Bacillus clade; ec, Escherichia–Synechocystis clade; ma, Methanococcus–Aquifex clade; and mf, Methanococcus–Archaeoglobus clade. A χ² test (see Methods) indicates that the distribution of roots is significantly different (P < 0.0039) for the two lineages.

Figure 3

The distribution of peripheral branch–transfer distances of operational and informational trees from the EF-1α reference tree. The mean distance of operational trees (A) is 2.3 steps, whereas the mean distance of the informational trees (B) is 1.2 steps. By the χ² test the two distributions are significantly different (P < 0.0003).

Figure 4

The distribution of prune-and-regraft distances of operational and informational trees from the reference tree. By the χ² test the two distributions are significantly different (P < 0.00007).

Figure 5

Phylogenetic trees indicating the local deviations of operational and informational trees from the reference tree. The average percentages of support for the alternative local topologies of the operational genes (A) and the informational genes (B) are indicated. The top number associated with each internal branch is the average support for the quartet shown and the bottom two values are for the two alternative topologies (see Methods).

Figure 6

Examples of the complexity of gene product interactions in informational genes (A) and operational genes (B). The assembly map (34) of the Escherichia, small ribosomal subunit is shown in A as an illustration of the high complexity that is frequently present in the translational apparatus. The thioredoxin (Th) and thioredoxin reductase (ThR) complex is shown in B as an example of the reduced complexity present in some operational genes.