Background: Although prevalent in prokaryotes, horizontal gene transfer (HGT) is rarer in
multicellular eukaryotes. Bdelloids rotifers are microscopic animals that contain a higher
proportion of horizontally transferred, non-metazoan genes in their genomes than typical of
animals. It has been hypothesized that bdelloids incorporate foreign DNA when they repair
their chromosomes following double-strand breaks caused by desiccation. HGT might thereby
contribute to species divergence and adaptation, as in prokaryotes. If so, we expect that
species should differ in their complement of foreign genes, rather than sharing the same set of
foreign genes inherited from a common ancestor. Furthermore, there should be more foreign
genes in species that desiccate more frequently. We tested these hypotheses by surveying
HGT in four congeneric species of bdelloids from different habitats: two from permanent
aquatic habitats and two from temporary aquatic habitats that desiccate regularly.
Results: Transcriptomes of all four species contain many genes with a closer match to nonmetazoan
genes than to metazoan genes. Whole genome sequencing of one species confirmed
the presence of these foreign genes in the genome. Nearly half of foreign genes are shared
between all four species and an outgroup from another family, but many hundreds are unique
to particular species, which indicates that HGT is ongoing. Using a dated phylogeny, we
estimate an average of 12.8 gains versus 2.0 losses of foreign genes per million years.
Consistent with the desiccation hypothesis, the level of HGT is higher in the species that
experience regular desiccation events than those that do not. However, HGT still contributed
hundreds of foreign genes to the species from permanently aquatic habitats. Foreign genes
were mainly enzymes with various annotated functions that include catabolism of complex
polysaccharides and stress responses. We found evidence of differential loss of ancestral
foreign genes previously associated with desiccation protection in the two non-desiccating
species.
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Conclusions: Nearly half of foreign genes were acquired before the divergence of bdelloid
families over 60Mya. Nonetheless, HGT is ongoing in bdelloids and has contributed to
putative functional differences among species. Variation among our study species is
consistent with the hypothesis that desiccating habitats promote HGT.