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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

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).
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Fig3: 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).

Mentions: Among these examples, we reclaim those encoding the hyaluronan synthases (HAS1-3). These were originally proposed as examples of prokaryote-to-metazoan HGT [19], but later rejected [20]; however, neither study considered foreign taxa other than bacteria. We were able to identify all three hyaluronan synthases as class A HGT, originating from fungi, an assessment supported by our phylogenetic analysis (FigureĀ 3). The HAS genes appear in a wide variety of chordates, but not in non-chordate metazoans, suggesting they result from the transfer of a single gene around the time of the common ancestor of Chordata, before undergoing duplications to produce the three genes found in primates. As the original rebuttal paper [20] only focused on recent HGT, and did not look for eukaryotic matches outside Chordata, they could not detect this ancient HGT.Figure 3


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)

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

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

Fig3: 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).
Mentions: Among these examples, we reclaim those encoding the hyaluronan synthases (HAS1-3). These were originally proposed as examples of prokaryote-to-metazoan HGT [19], but later rejected [20]; however, neither study considered foreign taxa other than bacteria. We were able to identify all three hyaluronan synthases as class A HGT, originating from fungi, an assessment supported by our phylogenetic analysis (FigureĀ 3). The HAS genes appear in a wide variety of chordates, but not in non-chordate metazoans, suggesting they result from the transfer of a single gene around the time of the common ancestor of Chordata, before undergoing duplications to produce the three genes found in primates. As the original rebuttal paper [20] only focused on recent HGT, and did not look for eukaryotic matches outside Chordata, they could not detect this ancient HGT.Figure 3

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