Lateral transfer of genes and gene fragments in prokaryotes

Abstract

Lateral genetic transfer (LGT) involves the movement of genetic material from one lineage into another and its subsequent incorporation into the new host genome via genetic recombination. Studies in individual taxa have indicated lateral origins for stretches of DNA of greatly varying length, from a few nucleotides to chromosome size. Here we analyze 1,462 sets of single-copy, putatively orthologous genes from 144 fully sequenced prokaryote genomes, asking to what extent complete genes and fragments of genes have been transferred and recombined in LGT. Using a rigorous phylogenetic approach, we find evidence for LGT in at least 476 (32.6%) of these 1,462 gene sets: 286 (19.6%) clearly show one or more "observable recombination breakpoints" within the boundaries of the open reading frame, while a further 190 (13.0%) yield trees that are topologically incongruent with the reference tree but do not contain a recombination breakpoint within the open reading frame. We refer to these gene sets as observable recombination breakpoint positive (ORB(+)) and negative (ORB(-)) respectively. The latter are prima facie instances of lateral transfer of an entire gene or beyond. We observe little functional bias between ORB(+) and ORB(-) gene sets, but find that incorporation of entire genes is potentially more frequent in pathogens than in nonpathogens. As ORB(+) gene sets are about 50% more common than ORB(-) sets in our data, the transfer of gene fragments has been relatively frequent, and the frequency of LGT may have been systematically underestimated in phylogenetic studies.

Keywords: comparative genomics; genetic recombination; genome evolution; horizontal genetic transfer; lateral genetic transfer.

FIG. 1.—

Definition of ORB⁺ and ORB⁻ gene sets. This simplified example shows six cases of LGT, each involving an orthologous region of six genomes (the white rectangles); adjacent genes A and B lie fully within this region in each genome, with gene boundaries as shown by the vertical dashed lines. Each case 1–6 corresponds to the presence of a single genetically recombined region (colored in red); thus, for the LGT event depicted in case 4, a recombination breakpoint is detected in gene set A (but not in gene set B), and the tree inferred for gene set B is topologically incongruent with the reference tree. We therefore label gene set A as ORB⁺ and gene set B as ORB⁻ as shown in the table on the right. ORB⁺ cases are shaded in light blue.

FIG. 2.—

Size distribution of (A) ORB⁺ and (B) ORB⁻ gene sets. The solid red bars indicate overrepresented size classes; the solid blue bars indicate underrepresented classes; and the gray bars indicate classes neither over- nor underrepresented in comparison with the corresponding size-class frequency over all 1,462 gene sets, at P ≤ 0.05.

FIG. 3.—

Representation of functional categories assigned to protein sequences corresponding to the (A) ORB⁺ and (B) ORB⁻ gene sets (solid yellow bars). The solid blue bars show the representation of these same functional categories in the full data set (16,639 gene sets of size ≥4, 119,695 proteins). Categories are numbered (differently for A and B) as shown in the boxes. Significance of over- or underrepresentation is represented by single (P ≤ 0.05) and double asterisks (P ≤ 0.01).

FIG. 4.—

Taxonomic origins (National Center for Biotechnology Information level-4 taxa) of genes in the (A) ORB⁺ and (B) ORB⁻ gene sets. Overrepresentation relative to the 16,639 gene sets is shown in red; underrepresentation is shown in blue; gray indicates that there is neither over- nor underrepresentation at P ≤ 0.05.