Bdelloid rotifers are microinvertebrates with unique characteristics: they have survived tens of millions of years without sexual reproduction; they withstand extreme desiccation by undergoing anhydrobiosis; and they tolerate very high levels of ionizing radiation. Recent evidence suggests that subtelomeric regions of the bdelloid genome contain sequences originating from other organisms by horizontal gene transfer (HGT), of which some are known to be transcribed. However, the extent to which foreign gene expression plays a role in bdelloid physiology is unknown. We address this in the first large scale analysis of the transcriptome of the bdelloid Adineta ricciae: cDNA libraries from hydrated and desiccated bdelloids were subjected to massively parallel sequencing and assembled transcripts compared against the UniProtKB database by blastx to identify their putative products. Of ∼29,000 matched transcripts, ∼10% were inferred from blastx matches to be horizontally acquired, mainly from eubacteria but also from fungi, protists, and algae. After allowing for possible sources of error, the rate of HGT is at least 8%–9%, a level significantly higher than other invertebrates. We verified their foreign nature by phylogenetic analysis and by demonstrating linkage of foreign genes with metazoan genes in the bdelloid genome. Approximately 80% of horizontally acquired genes expressed in bdelloids code for enzymes, and these represent 39% of enzymes in identified pathways. Many enzymes encoded by foreign genes enhance biochemistry in bdelloids compared to other metazoans, for example, by potentiating toxin degradation or generation of antioxidants and key metabolites. They also supplement, and occasionally potentially replace, existing metazoan functions. Bdelloid rotifers therefore express horizontally acquired genes on a scale unprecedented in animals, and foreign genes make a profound contribution to their metabolism. This represents a potential mechanism for ancient asexuals to adapt rapidly to changing environments and thereby persist over long evolutionary time periods in the absence of sex.
Bdelloid rotifers are tiny invertebrates with unusual characteristics: they withstand stresses, such as desiccation and high levels of ionising radiation, that kill other animals, and they have survived over millions of years without sexual reproduction, which contradicts theories on the evolutionary advantages of sex. In this study, we investigate another bizarre feature of bdelloids, namely their ability to acquire genes from other organisms in a process known as horizontal gene transfer (HGT). We show that HGT happens on an unprecedented scale in bdelloids: approximately 10% of active genes are “foreign,” mostly originating from bacteria and other simple organisms like fungi and algae, but now functioning as bdelloid genes. About 80% of foreign genes code for enzymes, and these make a major contribution to bdelloid biochemistry: 39% of enzyme activities have a foreign contribution, and in 23% of cases the activity in question is uniquely specified by a foreign gene. This indicates biochemistry, such as toxin degradation and antioxidant generation, that is unknown in other animals and that is expected to improve the “robustness” of the bdelloid. It also represents a possible mechanism for survival without sex, by diversification of functional capacity and even replacement of defective genes by foreign counterparts.