Horizontal Gene Transfer and Kleptoplasty
By Ferris Jabr is a freelance science journalist, on Aeon.Co
The first hints of horizontal gene transfer among complex organisms emerged several decades ago. In the 1940s, at Cold Spring Harbor Laboratory in New York, Barbara McClintock discovered that certain genes in corn plants could pop out of one position on a chromosome and move to another. The extent to which this transposition happened in a particular kernel determined its unique pattern of colourful speckles. McClintock’s pioneering work demonstrated for the first time that a genome is highly dynamic, not forever fixed in one order.
That was a difficult concept for many scientists to accept. By the 1970s, however, other researchers had discovered ‘jumping genes’, or transposons, in much more than just corn, and the scientific community at large finally began to celebrate McClintock’s work, which earned her the Nobel Prize in 1983. Scientists now know that transposons are extremely abundant and often constitute large portions of a given genome: they make up more than 85 per cent of the maize genome and about half of our own. Some slice themselves out of one spot on a chromosome and move to another; others take a copy-and-paste approach, quickly multiplying. To make these jumps, transposons rely on two main strategies: either they include a genetic sequence encoding an enzyme known as transposase, which can chop a transposon out of its current location and reintroduce it elsewhere; or they use a different set of enzymes to produce strings of RNA that are translated into DNA and woven back into the host genome.
Horizontal gene transfer was partly responsible for reproductively isolating lab-bred populations of fruit flies from wild ones – a major step on the way towards speciation. Still, most biologists viewed horizontal gene transfer among insects and other animals as something of an anomaly. Yes, bacteria and viruses exchanged DNA on a daily basis. But when it came to animals, plants and fungi, such genetic trespassing was surely rare overall and, in most cases, of little importance.
These are exactly the notions that have unravelled in the past decade as researchers have turned up one new case of gene transfer after another. ‘There was a time when we didn’t even realise that transposons could come from other species,’ says Cedric Feschotte of the University of Utah. ‘Now it seems our own genome is a patchwork of raw genetic material coming from different places with different histories – that to me is very profound. Even the largest eukaryote genomes have this patchwork origin to them.’
In the mid-2000s, Feschotte and his colleagues noticed some unusual patterns among the sequenced genomes of various mammals. Again and again, the lineage of certain DNA segments failed to align with established evolutionary relationships. They would find, for example, nearly identical sequences of DNA in mice and rats, but not in squirrels; and the same sequence would turn up in nocturnal primates known as bushbabies, but not in other primate species. It was highly unlikely that mice, rats and bushbabies had independently evolved the exact same chunk of DNA. Further complicating things, these puckish strings of DNA were not in the same position on the same chromosome in different species, as you would expect if they had been inherited the traditional way – rather, their locations were highly variable….
The reason, Feschotte and colleagues discovered in 2008, is that these DNA sequences were not vertically inherited genes; rather, they belonged to a widespread family of transposons, which the scientists dubbed SPACE INVADERS, or SPINs for short. SPINs have managed to insert themselves into the genomes of tenrecs, little brown bats, opossums, green anole lizards and African clawed frogs, in addition to bushbabies, mice and rats. In each of these species’ genomes, the transposons have multiplied either themselves or abbreviated forms of themselves thousands of times. And, in at least one case, mice and rats have adopted a SPIN transposon as one of their own, turning it into a functional gene that is actively read by the cellular machinery that translates genes into proteins, though its exact role remains a mystery. Over the past 30 million years, several SPINs have infiltrated the little brown bat’s genome and replicated an enormous number of times. This amplification coincides with one of the swiftest periods of speciation in the bat’s evolutionary history. It is by no mean’s conclusive proof that horizontal gene transfer encouraged the speciation, but it is indicative.
A different kind of transposon – one of the copy-and-paste variety – has spread through an equally diverse group of animals. In 2012, David Adelson, Ali Walsh at the University of Adelaide, and their colleagues, discovered that the transposon BovB – first found in cows (hence the bovine epithet) – is also present in anoles, opossums, platypuses, wallabies, horses, sea urchins, silkworms and zebrafish, to name a few. Once again, vertical inheritance via traditional evolutionary relationships could not explain the transposon’s haphazard materialisation here and there. On its epic journey through the tree of life, BovB has jumped between species at least nine times, and seems to have generally moved from reptiles to mammals.
How does one little piece of DNA get into all those distantly related creatures living in such different places – animals that likely never even encountered one another, let alone mated? It probably enlists the help of organisms that have mastered the art of hitchhiking: ticks. Adelson, Walsh and colleagues found BovB in several tick species known to vampirise reptiles. Likewise, a couple of years after first discovering SPINs, Feschotte and colleagues found them yet again in two creatures that – just like the mite with an appetite for fruit fly eggs – have the potential to transmit transposons from one animal to another: a blood-sucking insect known as the kissing bug (Rhodnius prolixus), which feeds on birds, mammals and reptiles alike; and the pond snail (Lymnaea stagnalis), which is host to many parasitic flatworms that infect various vertebrates. Alone, the kissing bug and pond snail cannot explain all of SPINs’ conquests; their habitats overlap with many but not all of the vertebrates that contain the transposons. But the available evidence suggests that this six-legged parasite and shelled parasite hotel are two key accomplices that allowed SPINs to infiltrate so many different animal lineages within the past 50 million years.
Sometimes, parasites transfer far more than a single gene into the genomes of their hosts. Like many insects, the fruit fly species Drosophila ananassae is home to parasitic bacteria known as wolbachia, typically found in an insect’s sex organs. Through a series of gene‑sequencing studies, scientists have confirmed that the wolbachia species living inside D ananassae has shuttled not just one, but all of its 1,206 genes into the fruit fly’s DNA. Consider this: insects are collectively the most numerous animals on the planet; wolbachia infects between 25 and 70 per cent of all insect species, and it’s probable that wolbachia has successfully completed such genetic mergers in far more than fruit flies. Think of the quintillions of insects in the world – all those buzzing, bristling, bug-eyed creatures. At their very core, most of them might not be individual organisms but at least two beasts in one.
Recently, while studying a virus that preys on wolbachia, Jason Metcalf and Seth Bordenstein of Vanderbilt University in Tennessee discovered the Napoleon of horizontal gene transfers: a little gene that has conquered every kingdom of life. The virus in question attacks and kills wolbachia using a gene named GH25-muramidase, which encodes an enzyme that can perforate bacterial cell walls. When Metcalf and Bordenstein traced the evolutionary lineage of GH25, they discovered a pattern of inheritance that looked anything but typical. The GH25 gene was scattered throughout the tree of life: in bacteria, plants, fungi and insects. This particular gene seems to have moved fluidly through the microbial world and then hopped laterally to viruses, plants, fungi and insects living in close association with different kinds of bacteria. ‘Every organism needs to fight bacteria off,’ Metcalf says. ‘If they can get a new method of antibacterial defence, that’s a huge evolutionary advantage for them.’…
…Shake any branch on the tree of life and another astonishing case of interspecies gene transfer will fall at your feet. Bdelloid rotifers – tiny translucent animals that look something like sea slugs – have constructed a whopping eight per cent of their genome using genes from bacteria, fungi and plants. Fish living in icy seawater have traded genes coding for antifreeze proteins. Gargantuan-blossomed rafflesia have exchanged genes with the plants they parasitise. And in Japan, some people’s gut bacteria have stolen seaweed-digesting genes from ocean bacteria lingering on raw seaweed salads.
At this point, the tally is too high to ignore. Scientists can no longer write off gene-swapping among eukaryotes – and between prokaryotes and eukaryotes – as inconsequential. Clearly genes have all kinds of ways of journeying between the kingdoms of life: sometimes in large and sudden leaps; other times in incremental steps over millennia. Granted, many of these voyages are probably futile: a translocated gene finds itself to be utterly useless in its new home, or becomes such a nuisance to its genetic neighbours that it is evicted. Laterally transferred genes can be imps of chaos, gumming up or refashioning a genome in a way that is ultimately disastrous – perhaps even lethal to a species. In a surprising number of instances, however, wayfaring genes make a new life for themselves, becoming successful enough to change the way an organism behaves and steer its evolution.
The fact that horizontal gene transfer happens among eukaryotes does not require a complete overhaul of standard evolutionary theory, but it does compel us to make some important adjustments. According to textbook theories of evolution, the major route of genes moving between organisms is parent to child – whether through sex or asexual cloning – not this sneaky business of escorting genes between unrelated organisms. We must now acknowledge that, even among the most complex organisms, vertical is not the only direction in which genes travel.
Likewise, standard theory says that mutations are supposed to happen within a species’s own genome, not come from somewhere else entirely. We now know that the appearance of new genes does not necessarily result from tweaks to native DNA, but might instead represent the arrival of far-flung visitors. ‘We need to start thinking about genomes as ecological units rather than monolithic units,’ says Jack Werren of the University of Rochester in New York, one of the scientists who discovered the wolbachia/fruit fly Russian doll. ‘We’re dealing with a new category by which unique genes can evolve.’
In some cases, this genetic hopscotching ‘could exert a very powerful evolutionary force’, says Li. ‘It can introduce novelties that cannot be achieved by gradual genetic mutations.’ Consider that a plant acquiring a gene from a bacterium, or an aphid from a fungus, is not receiving some half-constructed genetic prototype. Rather, it gets the benefit of all the aeons of natural selection that have whittled that gene in another creature, honing its power. An introduced gene might need some tweaks before it whirs in sync with its new neighbours, but it could be closer to such harmony than a de novo mutation that was caused by, say, a cell-division error or UV radiation. Horizontal gene transfer opens the possibility of a creature instantaneously acquiring a gene-trait combo that its own genome would have been unlikely to invent by itself.
Many animal genomes include bacterial and fungal genes acquired by horizontal gene transfer (HGT) during evolution, according to a study published today (March 12) in Genome Biology. Scanning the genomes of fruit flies, nematodes, primates, and humans, among other animals, researchers found evidence to suggest that some of these horizontally acquired genes may even be functional.
When the human genome was first published, the suggestion that it contained bacterial genes was controversial. Subsequent studies questioned the possibility of HGT, offering alternate explanations for the presence of genes that resembled bacterial sequences, such as gene loss, or convergent or divergent evolution.
“There were methodological issues with both sides of the argument, and the main problem was that we just didn’t have the data back then that we do now,” said Alastair Crisp of the University of Cambridge, an author on the new study.
More recently, several researchers have reported the lateral transfer of bacterial genes into metazoans under specific circumstances. Examples include the interaction of insect hosts with the obligate intracellular parasite Wolbachia, or the transfer of subsets of bacterial genes into specific kinds of cells, such as cancer cells.
But this latest study is the first to extend across a breadth of species and types of genes. “The study makes a compelling case presenting more evidence of lateral gene transfer from bacteria into eukaryotes,” said microbiologist Julie Hotopp of the University of Maryland who was not involved with the work. “Redoing this type of analysis has been needed for quite some time. People continue to cite the papers from 2000 and 2001 as examples that there is no lateral gene transfer, particularly in humans.”
LS4. Biological Evolution: Unity and Diversity
HS-LS4-5. Evaluate models that demonstrate how changes in an environment may result in the evolution of a population of a given species, the emergence of new species over generations, or the extinction of other species due to the processes of genetic drift, gene flow, mutation, and natural selection
AP Biology, Essential Knowledge 3.C.2
- b. The horizontal acquisitions of genetic information primarily in prokaryotes via transformation (uptake of naked DNA), transduction (viral transmission of genetic information), conjugation (cell-to-cell transfer) and transposition (movement of DNA segments within and between DNA molecules) increase variation.