Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae

Abstract

SUMMARYBdelloid rotifers are aquatic micro-invertebrates with the ability to survive extreme desiccation, or anhydrobiosis, at any life stage. To gain insight into the molecular mechanisms used by bdelloids during anhydrobiosis, we constructed a cDNA library enriched for genes that are upregulated in Adineta ricciae 24h after onset of dehydration. Resulting expressed sequence tags (ESTs) were analysed and sequences grouped into categories according to their probable identity. Of 75 unique sequences, approximately half (36) were similar to known genes from other species. These included genes encoding an unusual group 3 late embryogenesis abundant protein, and a number of other stress-related and DNA repair proteins. Open reading frames from a further 39 novel sequences, without counterparts in the database, were screened for the characteristics of intrinsically disordered proteins, i.e. hydrophilicity and lack of stable secondary structure. Such proteins have been implicated in desiccation tolerance and at least five were found. The majority of the genes identified was confirmed by real-time quantitative PCR to be capable of upregulation in response to evaporative water loss. Remarkably, further database and phylogenetic analysis highlighted four ESTs that are present in the A. ricciae genome but which represent genes probably arising from fungi or bacteria by horizontal gene transfer. Therefore, not only can bdelloid rotifers accumulate foreign genes and render them transcriptionally competent, but their expression pattern can be modified for participation in the desiccation stress response, and is presumably adaptive in this context. Supplementary material available online at

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…In this sense, some of the genes acquired by Adineta ricciae seem to be upregulated by water loss, suggesting that they might be involved in the desiccation stress response [24].…”

Trafficking of bdelloid rotifer late embryogenesis abundant proteins

“…ArLEA1A and ArLEA1B are group 3 LEA proteins encoded by the genes Ar-lea-1A and Ar-lea-1B, respectively, first identified in a cDNA population isolated from desiccating A. ricciae (PouchkinaStantcheva et al, 2007;Boschetti et al, 2011). Comparison of ArLEA1A and ArLEA1B protein sequences has revealed that they differ at only 12 of their matching amino acid positions.…”

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

“…Functional horizontal gene transfer (fHGT) can bring to a recipient genome new biochemical capacities and contrasts with gradualist evolution of endogenous genes to new function. The bdelloid rotifers Adineta vaga (28) and Adineta ricciae (29) have high levels of fHGT (∼8%), and this has been associated with both their survival as phylogenetically ancient asexuals and their ability to undergo cryptobiosis (28)(29)(30)(31)(32). Different kinds of evidence are required to support claims of doaHGT compared with fHGT.…”