Virus-like transposons cross the species barrier and drive the evolution of genetic incompatibilities

• 成果类型: Article
• 署名作者: Widen, Sonya A. A.; Bes, Israel Campo; Koreshova, Alevtina; Pliota, Pinelopi; Krogull, Daniel; Burga, Alejandro
• 署名单位: Vienna Biocenter (VBC); Institute of Molecular Biotechnology (IMBA); Medical University of Vienna; University of Vienna; Vienna Biocenter (VBC); Medical University of Vienna; Barcelona Institute of Science & Technology; Pompeu Fabra University; Centre de Regulacio Genomica (CRG)
• 刊物名称: SCIENCE
• ISSN/ISSBN: 0036-12933
• DOI: 10.1126/science.ade0705
• 发表日期: 2023-06-23
• 页码: 1336-+
• 关键词: horizontal transfer; ELEMENTS; CONSERVATION; eukaryotes; algorithm; virophage; proteases; vectors; FAMILY

摘要

INTRODUCTION When we think of DNA, we think of inheritance from parent to offspring. However, DNA can also be transmitted between individuals that are not related and even between individuals belonging to different species in a process known as horizontal gene transfer (HGT). Although best characterized in bacteria, a growing body of evidence indicates that HGT can also take place in a wide range of eukaryotes, including fungi, plants, and animals. However, one of the most fascinating aspects of HGT, the mechanism of transfer in metazoans, remains largely uncharacterized.RATIONALE Many microorganisms can take up DNA from their environment, and some have even evolved specialized machinery to transfer DNA between peers. In sharp contrast, transfer of DNA between multicellular organisms poses a greater logistical challenge. For HGT to take place, DNA must first find its way out of the donor species, come in close contact with the germ line of a second species (which is physically and molecularly guarded), and, finally, integrate into the genome of the new host. Viruses have long been hypothesized to mediate HGT because of their known ability to take up DNA sequences from their hosts, integrate into genomes, and infect different species. However, evidence is sparse and mostly limited to highly specialized viral symbionts that have co-evolved in the genomes of parasitoid wasps.RESULTS While studying nematodes, we discovered one of the long-sought vectors of HGT in eukaryotes: Maverick elements. Mavericks, also known as Polintons, are unique because they share features of both transposons and viruses. Like transposons, Mavericks are flanked by terminal inverted repeats and can readily jump and insert into genomes. Like viruses, they code for a large number of proteins, including a type-B DNA polymerase, a retroviral-like integrase, as well as major and minor capsid proteins. We discovered that two new nematode gene families, wosp proteases and krma kinases, are preferentially taken up as cargo by Mavericks and have been extensively transferred between different nematode species on a global scale. Many of these transfers occurred between species that last shared a common ancestor likely hundreds of millions of years ago. We also found that nematode Mavericks captured a new fusogen, MFUS-1 (for Maverick fusogen), which is structurally most similar to the glycoprotein B from Herpes simplex virus 1. This event likely fueled the spread of Mavericks through the formation of enveloped infective particles, analogous to the inception of retroviruses from genomic retroelements. Finally, we show how the union between a horizontally transferred wosp protease, msft-1, and a MULE (Mutator-like elements) transposon gave birth to a new class of selfish gene in the nematode Caenorhabditis briggsae: a mobile toxin-antidote element that causes genetic incompatibilities in wild populations.CONCLUSION Our study illustrates how the intertwined biology of viruses and transposons can ultimately affect gene flow between populations. Indeed, HGT can result in regions of high sequence similarity between distantly related populations, masquerading as selection or introgression. Although different vectors of HGT likely exist in nature, we predict that Mavericks, and analogous transposable elements with viral properties, could mediate HGT in other animal eukaryotic lineages, including vertebrates.Mavericks mediate HGT between nematodes.(A) Mavericks share features of both transposable elements and viruses.