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

Crisp A, Boschetti C, Perry M, Tunnacliffe A, Micklem G - Genome Biol. (2015)

Bottom Line: 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.We also resolve the controversy surrounding previous evidence of HGT in humans and provide at least 33 new examples of horizontally acquired genes.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.

View Article: PubMed Central - PubMed

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.

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Related in: MedlinePlus

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 horth, 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).
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Fig2: 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 horth, 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).

Mentions: We first identified a base level of HGT (called class C) by using conservative thresholds of h ≥30 (as in [12]) (meaning that the gene aligns much better, and is therefore much more similar, to non-metazoan genes) and bitscore of best non-metazoan match ≥100 (thereby excluding bad alignments to non-metazoans). The example given above (gob-1) passes these thresholds and is therefore at least class C HGT. This per-species information was then combined for each taxon (Drosophila, Caenorhabditis and primates) to construct ortholog groups. For each ortholog group we calculated the average h value of all members (horth) and defined the genes with horth ≥30 as class B, a subset of class C. These genes are, on average, predicted as HGT in all tested species they are found in. The gene gob-1 has homologs in C. brenneri, C. briggsae and C. japonica, with values of h = 102, h = 97.1 and h = 86.4 respectively, giving an average h (horth) of 95.3 and as such gob-1 (ands its homologs) are also class B HGT. Finally, we applied a still more stringent filter to define class A foreign genes (a subset of class B), which had only very poor alignments to metazoan sequences and whose orthologs, as used to define class B, also had similarly poor alignments to metazoan sequences. To do this, we identified those sequences whose best match to a metazoan had a bitscore <100 and whose ortholog groups contain no genes with metazoan matches of bitscore ≥100 (Figure 2A). The gene gob-1 has no metazoan matches with bitscore ≥100 (best metazoan match = 39.3) and the same is true for its homologs (best matches of 37, 38.9 and 36.6, respectively), as such it is also class A HGT.Figure 2


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

Crisp A, Boschetti C, Perry M, Tunnacliffe A, Micklem G - Genome Biol. (2015)

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 horth, 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).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4358723&req=5

Fig2: 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 horth, 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).
Mentions: We first identified a base level of HGT (called class C) by using conservative thresholds of h ≥30 (as in [12]) (meaning that the gene aligns much better, and is therefore much more similar, to non-metazoan genes) and bitscore of best non-metazoan match ≥100 (thereby excluding bad alignments to non-metazoans). The example given above (gob-1) passes these thresholds and is therefore at least class C HGT. This per-species information was then combined for each taxon (Drosophila, Caenorhabditis and primates) to construct ortholog groups. For each ortholog group we calculated the average h value of all members (horth) and defined the genes with horth ≥30 as class B, a subset of class C. These genes are, on average, predicted as HGT in all tested species they are found in. The gene gob-1 has homologs in C. brenneri, C. briggsae and C. japonica, with values of h = 102, h = 97.1 and h = 86.4 respectively, giving an average h (horth) of 95.3 and as such gob-1 (ands its homologs) are also class B HGT. Finally, we applied a still more stringent filter to define class A foreign genes (a subset of class B), which had only very poor alignments to metazoan sequences and whose orthologs, as used to define class B, also had similarly poor alignments to metazoan sequences. To do this, we identified those sequences whose best match to a metazoan had a bitscore <100 and whose ortholog groups contain no genes with metazoan matches of bitscore ≥100 (Figure 2A). The gene gob-1 has no metazoan matches with bitscore ≥100 (best metazoan match = 39.3) and the same is true for its homologs (best matches of 37, 38.9 and 36.6, respectively), as such it is also class A HGT.Figure 2

Bottom Line: 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.We also resolve the controversy surrounding previous evidence of HGT in humans and provide at least 33 new examples of horizontally acquired genes.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.

View Article: PubMed Central - PubMed

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.

Show MeSH
Related in: MedlinePlus