Evidence for ancient horizontal gene acquisitions in bdelloid rotifers of the genus adineta

Until recently, obligate asexuality was often considered an evolutionary dead end. However, recent advances suggest that conventional sexual reproduction, defined as the alternation of meiosis and fertilization, is not the only sustainable eukaryotic lifestyle. Moreover, different modes of asexual reproduction are observed in nature, raising the question of the diverse mechanisms responsible for the long-term survival and adaptation of strict asexuals. One possible way to study the molecular-genetic consequences of the loss of meiotic recombination is to scrutinize the genomes of asexuals of ancient and more recent origins. The first genome draft of an ancient asexual species, the bdelloid rotifer Adineta vaga, was recently made available, revealing a peculiar genomic structure in which allelic regions were massively rearranged and sometimes found on the same chromosome. Such genome organization devoid of homologous chromosomes appears incompatible with meiotic pairing and segregation, and represents therefore a compelling genomic signature of asexuality. Besides, the genome of A. vaga contains around 8% of genes of apparent nonmetazoan origin, a percentage much higher than observed in most eukaryotes. Interestingly, a similar percentage of genes of nonmetazoan origin was independently inferred from a large-scale transcriptome analysis of the bdelloid rotifer Adineta ricciae. In this chapter, we conducted a comparative study between these two closely related species using reciprocal best blast hits, followed by functional annotation using the GOANNA pipeline. Around 10% of all the orthologs identified between the two species were putatively acquired by horizontal gene transfer and lots of them were associated to hydrolases (18%) and oxidoreductases (16%) functions. We hypothesize that these acquisitions may have helped bdelloids to adapt to multiple food sources and to develop enhanced resistance to desiccation. Furthermore, comparisons with sequences available for the monogonont rotifer Brachionus plicatilis suggest that some nonmetazoan genes were acquired by rotifers before the separation of bdelloids and monogononts.