Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes

Abstract

Background: A fundamental concept in biology is that heritable material, DNA, is passed from parent to offspring, a process called vertical gene transfer. An alternative mechanism of gene acquisition is through horizontal gene transfer (HGT), which involves movement of genetic material between different species. HGT is well-known in single-celled organisms such as bacteria, but its existence in higher organisms, including animals, is less well established, and is controversial in humans.

Results: We have taken advantage of the recent availability of a sufficient number of high-quality genomes and associated transcriptomes to carry out a detailed examination of HGT in 26 animal species (10 primates, 12 flies and four nematodes) and a simplified analysis in a further 14 vertebrates. Genome-wide comparative and phylogenetic analyses show that HGT in animals typically gives rise to tens or hundreds of active 'foreign' genes, largely concerned with metabolism. Our analyses suggest that while fruit flies and nematodes have continued to acquire foreign genes throughout their evolution, humans and other primates have gained relatively few since their common ancestor. We also resolve the controversy surrounding previous evidence of HGT in humans and provide at least 33 new examples of horizontally acquired genes.

Conclusions: We argue that HGT has occurred, and continues to occur, on a previously unsuspected scale in metazoans and is likely to have contributed to biochemical diversification during animal evolution.

Figure 1

Phylogenetic relationships of the main taxonomic groups studied. The blue numbers indicate the ortholog groups mapping to each branch (HGT events). Events may have occurred anywhere along the branch, not just where the number is indicated. Events found at the base of the tree have occurred anywhere between the origin of the phylum and the base of the tree. Trees are not drawn to scale with each other.

Figure 2

HGT genes by class. ( A ) The left panel shows a schematic representation of the HGT classes: class B and C genes have h index ≥ 30 and bitscore of the best non-metazoan blastx hit ≥ 100 (they are distinguished by h _orth, which is not shown on this figure), while class A genes must additionally have bitscore <100 for the best metazoan blastx hit. The right panel shows the scores for all genes in H. sapiens, colour-coded according to their classification (class A: red, class B: orange, class C: blue, native genes: grey). ( B ) Box-plot of the number of genes in each class, for the three main taxa analysed (Drosophila spp. Caenorhabditis spp., primates species), colour-coded according to the same scheme (class A: red, class B: orange, class C: blue).

Figure 3

Phylogenetic tree for the human gene HAS1. For each branch the species name and UniProt accession is shown. The human gene under analysis is shown in orange, proteins from chordates are in red, other metazoa in black, fungi in pink, plants in green, protists in grey, archaea in light blue and bacteria in dark blue. Numbers indicate aLRT support values for each branch where higher than 0.75 (on short terminal branches the support values are not shown).

Figure 4

Mean origin of class C foreign genes for each taxon. Numbers show percentage contribution within each taxon (row). The same analyses for Class B or A genes show very similar patterns. The colour scheme is as in Figure 3: origin from archaea is light blue, from bacteria is dark blue, from protists is grey, from plants is green and from fungi is pink.