Abstract
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.
Highlights
Bdelloid rotifers (Rotifera, Bdelloidea) are abundant, ubiquitous microinvertebrates that inhabit aqueous habitats [1]
We present the first global analysis of the transcriptome of a bdelloid rotifer, A. ricciae, which shows that horizontally acquired genes are expressed on a scale unprecedented in animals and that they make a profound contribution to bdelloid metabolism
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
Summary
Bdelloid rotifers (Rotifera, Bdelloidea) are abundant, ubiquitous microinvertebrates that inhabit aqueous habitats [1]. The bdelloids Adineta vaga and Philodina roseola contain foreign DNA sequences in at least some subtelomeric chromosomal regions of their genomes, and these probably derive from horizontal gene transfer (HGT) [8] Three of these genes were shown to be transcribed, and Boschetti et al [9] showed that in a related bdelloid species, A. ricciae, four different foreign genes, out of a set of 36 identifiable foreign and native sequences sampled, were expressed. The proportion of the bdelloid genome harbouring foreign sequences, how many of these sequences are expressed, and their contributions to bdelloid physiology, are completely unknown To address these issues, we present the first global analysis of the transcriptome of a bdelloid rotifer, A. ricciae, which shows that horizontally acquired genes are expressed on a scale unprecedented in animals and that they make a profound contribution to bdelloid metabolism. We suggest this is highly significant in the context of the extremophile nature of bdelloids and their long term evolutionary persistence without sex, which theory suggests should limit their ability to adapt to changing environments [10,11,12,13]
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