To acquire new functions, evolution often relies on the creation of new genes. Well understood mechanisms of new gene creation include duplication, local mutation, and domain rearrangements. In some cases, however, genetic material can be acquired from exogenous DNA, a phenomenon known as horizontal gene transfer (HGT). oskar is a gene found only in the insect lineage that has evolved to be absolutely necessary for germ cell formation, and thus species survival, in some clades, including the fly Drosophila. Its evolutionary history, however, remains a mystery, as no homologs appear to exist outside the insect lineage. Here we elucidate the evolutionary origins of oskar, and show that oskar likely arose through a novel gene formation history. We used numerous recently published insect genomes and transcriptomes to analyze over 100 oskar sequences. We provide strong evidence that while one of oskar’s two conserved domains, the LOTUS domain, was present in an ancestral insect genome, the second one, the OSK domain, was acquired through a horizontal domain transfer from a bacterial GDSL-like lipase. Both domains would then have fused via conversion of intervening genomic DNA from non-coding to coding sequence,creating a new unique gene, which we hypothesize would have been the ancestral oskar sequence. Finally, we show that the OSK domain is related to GDSL-like lipases from a bacteria of a clade including to the genus Wolbachia, suggesting that bacterial endosymbionts could have provided source material for the HGT event that led to the genesis of oskar.
Alien invasion in the kingdom of insects
Leo Blondel, Cassandra G. Extavour
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This work was done at Harvard in the Molecular and Cellular Biology (MCB) department, Cambridge, MA, USA.
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