The movement of genetic material between different species, named horizontal gene transfer (HGT), is well-known in single-celled organisms such as bacteria. However, the process is less well established in multicellular organisms, in particular animals and humans. Research published in Genome Biology has found that actually HGT in multicellular organisms may be more common than previously thought. Here, we ask co-authors; Gos Micklem, Alastair Crisp, Chiara Boschetti and Alan Tunnacliffe, from the University of Cambridge, UK, about their research and what this could mean for animal evolution and human biology.
What is horizontal gene transfer (HGT) and what led to your interest in this area?
Vertical gene transfer (VGT) is the usual method of transmission of genetic information (DNA) from one generation to the next. In humans and other animals, the DNA is passed from parents to offspring through the germ line (eggs and sperm). By comparison, horizontal gene transfer (HGT) is the acquisition of a gene from an organism other than a parent. We refer to genes acquired by HGT as foreign genes, in contrast to native genes that have only ever been passed on by VGT.
We became interested in animal HGT after finding that bdelloid rotifers, small asexual animals resistant to dehydration, have an unusually high number of foreign genes. About ten percent of the active genes in bdelloids originally come from other organisms, such as bacteria and fungi.
Until now, the role of HGT in animal evolution was thought to be quite minor. Why has this been the case, and what makes now an ideal time to revisit this idea?
In multicellular organisms such as animals, HGT must occur in the small subset of cells that make up the germ line, otherwise, the newly acquired DNA will not be passed on to subsequent generations. This makes HGT events in animals much less likely than in single cell organisms such as bacteria, in which HGT is widespread. Furthermore, the germ line is usually protected from the environment, decreasing the probability of foreign DNA coming into contact with germ cells. The differences in genetic organisation between animals and bacteria may also make it more difficult for acquired genes to be functional.
In the human, and in model organisms (such as the fruit fly, D. melanogaster, and the roundworm, C. elegans), there have been few, if any, studies of HGT in the last decade. The increasing availability of genome, transcriptome and proteome data makes the accurate identification of HGT much easier than in the past. So this is an ideal time to re-examine HGT in animals.
How did the foreign genes find their way into animal genomes?
The exact mechanism is unclear, but HGT is likely to be the result of a succession of extremely rare events. It may involve the uptake of DNA molecules from the environment, probably from dead or dying organisms consumed in food. DNA is known to pass through biological membranes, and thus into cells, at low rates. There is then a very small chance that it will be integrated into the genome. This process is likely enhanced in dehydration-resistant organisms, like bdelloids, where the absence of water can cause membranes to leak and DNA to break. When DNA damage is repaired, some foreign genes may be incorporated into the genome. Another possibility is pathogen-mediated HGT.
What do the transferred genes do in their new hosts?
The genes have a variety of different functions, with the majority coding for enzymes. It is believed that genes whose protein products are involved in relatively few interactions with other biological molecules are more likely to be horizontally transferred and maintained. HGT may be a way for animals to acquire new biochemical functions, for example bdelloids have acquired genes to make essential amino acids, rather than having to acquire them in their diet.
Are there any implications from your findings about the role HGT may play in animal (metazoan) evolution as compared to bacterial evolution?
While our findings show that HGT is generally less widespread in animals than in bacteria, suggesting it plays a smaller role in animal evolution, we are still talking about tens to hundreds of foreign genes in each species we studied. Therefore, we cannot continue to ignore the potential contribution of HGT to animal evolution. HGT is more widespread in some species than in others and has occurred at different times in different animal lineages. For example, we found that the majority of the HGT in the primates is relatively ancient, so its effects on recent evolution may be limited.
What does HGT mean for human biology, and where can your results lead future research?
While the function of much HGT is unclear, some genes such as the ABO gene (involved in determining blood groups and previously found to be genetically transferred horizontally) play a major role in human biology. In the past, the presumption has been that similarity in genes is due to VGT, but our results mean HGT needs to be considered as well, even in complex organisms. In the future, studying the mechanisms underlining the acquisition of HGT may shed light on how genomes evolve.
Questions from Louisa Flintoft, Editor of Genome Biology.
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