Virus-like transposons wage war on the species barrier

A Maverick virus-like particle as a horizontal gene transfer (HGT) vector.  IMBA-IMP graphics

image: a Maverick virus-like particle as a horizontal gene transfer (HGT) vector. IMBA-IMP graphics
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Credit: IMBA-IMP graphics

Scientists have known for decades that genes can be transferred from one species to another, in both animals and plants. However, the mechanism of how such an unlikely event occurs has remained unknown. Now, researchers in Alejandro Burga’s lab at the Institute of Molecular Biotechnology (IMBA) of the Austrian Academy of Sciences have identified a horizontal gene transfer (HGT) vector in worms. The findings, published June 29 in Science, could lead to the discovery of additional HGT vectors in eukaryotes and could find applications in pathogen control.

Key points:

  • The transfer of genetic information between species, called horizontal gene transfer (HGT), is an obscure phenomenon reported in eukaryotes, including some vertebrate species. However, scientists have not been able to explain how this happens.
  • Now, researchers in Alejandro Burga’s lab at IMBA have discovered one of the long-sought vectors of HGT in nematodes: ancient virus-like transposons called Mavericks. They prove it Mavericks are responsible for an HGT event between two worm species whose genomes are as divergent as those of humans and fish.
  • Scientists predict it Mavericks and analogous elements could mediate HGT in a larger pool of animal lineages, including vertebrates.

Fish living in the Arctic and Antarctic oceans have developed ingenious strategies to keep their blood and tissue from freezing in the inhospitable polar waters. One such adaptive strategy is the evolution of genes that produce antifreeze proteins. However, over a decade ago, scientists were astounded to discover that herring and smelt — two completely different species — have the exact same antifreeze protein encoded in their genomes, indicating a gene transfer between them. Examples like this raise the question: how can genes “jump” between completely different species? This rare phenomenon, known as horizontal gene transfer (HGT), has puzzled evolutionary biologists for a long time. And although new cases of HGT have been discovered in all walks of life over the years, the mechanisms responsible for these transfers have remained largely unknown.

Now, scientists from Alejandro Burga’s group at IMBA not only catch an HGT event in the animal kingdom red-handed, but also identify one of its long-sought vectors. Using genetic investigation work, Burga and his team showed an HGT event between two reproductively isolated worm species that are genetically as different from each other as humans are from fish. . More importantly, they could identify what caused it: a family of virus-like transposons called Mavericks.

Nailing a culprit: Mavericks as vectors of HGT

“Mavericks were already known as a class of transposons, but our work links them for the first time to HGT,says IMBA group leader Alejandro Burga, corresponding author of the study. “We knew that HGT occurred between animal species, but we had no idea how. This is the first time we can finally nail a culprit,adds co-first author Sonya Widen, a postdoctoral fellow in the Burga lab.

When Mavericks were discovered in the mid-2000s, initially thought to be large transposons, selfish genetic elements that jump around and self-propagate in the genome at the expense of their host. Mavericks they were quickly reported in most branches of eukaryotes, including humans, thus establishing that they originated long ago.

Transposons and viruses, melting pot of nature?

Quick, try that Mavericks genes containing encoding viral elements, such as a capsid and a DNA polymerase, began to emerge. “The evolution of transposons and viruses is closely intertwined,Burga says. However, the capsid and DNA polymerase are not sufficient to allow a transposon to jump from its host’s genome and infect the cells of an entirely different host. Now, IMBA researchers have found the missing link: Mavericks in the genomes of worms they acquired a so-called fusion protein, a transmembrane protein that mediates membrane fusion between different cells. By acquiring afusigen, the authors hypothesize that the worm Mavericks it has become capable of forming virus-like particles that can fuse with another organism’s cell membranes and infect them. “To our knowledge, no fusegens have been reported in Mavericks Before. So, we think the worm Mavericks may have picked up their sequence from a virus,Widen says. “Transposons and viruses can be considered the melting pot of nature. Their union can have unpredictable repercussions and lead to genomic innovation,Burga says.

Demonstrating the significance of HGT in worms

In the present study, the IMBA team led by Alejandro Burga and co-first authors Sonya Widen and Israel Campo Bes, a former master’s student in the Burga lab, stumbled upon HGT “totally by accident,” Widen says. In fact, the team was studying the evolutionary origin of a selfish element in the nematode Caenorhabditis briggsae. By doing a little detective work, they were able to trace the sequence of this selfish gene back to another nematode, C. plicata, which carried an almost identical copy. This discovery is surprising because C. briggsae AND C. plicata they are two reproductively isolated species. “Their genomes are as divergent as those of humans and fish, yet both have a nearly identical gene that clearly shows features of an evolutionarily recent HGT event.” says Campo Bes. “Looking closely at the genome of C. plicatawe discovered that the ancestral sequence that gave rise to the selfish gene in C. briggsae was incorporated within a maverick In C. plicata. The fact that this newly introduced gene later evolved into a new selfish gene in C. briggsae demonstrates the impact of HGT on genome evolution,explains Widen. The IMBA team then continued to prove it Mavericks are responsible for dozens of independent HGT transfer events between worm species belonging to different genera and found worldwide.

Agricultural and medical relevance

IMBA scientists argue that transposon-virus binding is a key factor in mediating HGT. While still finding their success hard to believe, they recognize the impact their findings could have in unraveling the mysteries of HGT. “I was convinced we were looking at a case of HGT when we first saw these results in the lab, but I was also sure we would never find out how it happened. And yet, the stars aligned” says Burga, who foresees it too Mavericks and similar virus-like transposable elements could mediate HGT in vertebrates and other eukaryotes. Finally, the team envisions possible applications both in the laboratory and as pest control measures against parasitic worm species:Self maverickMediated HGT has been shown to be broadly applicable to any nematode species, it has the potential to become an invaluable resource. Beyond rigorous laboratory and research applications such as the genetic manipulation of non-model nematodes, such an asset could allow us, in the future, to genetically modify parasitic nematode species that may be of agricultural or medical significance,” concludes Burga.

Sonya A. Widen is a postdoctoral fellow at IMBA’s Burga laboratory and a member of the Vienna International Postdoctoral (VIP2) Fellowship Program at the Vienna BioCenter. Israel Campo Besformer master student in the Burga laboratory, he is currently doing a PhD at the Center for Genomic Regulation (CRG), Barcelona Institute of Science and TechnologyBarcelona, ​​Spain.

Original publication:

Sonya A. Widen*, Israel Campo Bes*, Alevtina Koreshova, Pinelopi Pliota, Daniel Krogull and Alejandro Burga, Virus-like transposons cross the species barrier and drive the evolution of genetic incompatibilities. Science (2023). DOI: https://doi.org/10.1126/science.ade0705

*Co-first authors

About IMBA:

The Institute of Molecular Biotechnology (IMBA) of the Austrian Academy of Sciences (ÖAW) is one of the leading biomedical research institutes in Europe. IMBA is located at the Vienna BioCenter, Austria’s vibrant group of universities, research institutes and biotech companies. IMBA research topics include chromosomal biology, RNA biology, selfish elements and silencing mechanisms, functional genomics, developmental and cell biology, stem cell biology, molecular medicine, neuroscience, organoid research, and disease modeling.


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