title: Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats.
abstract: BACKGROUND
  Although prevalent in prokaryotes, horizontal gene transfer (HGT) is rarer in multicellular eukaryotes. Bdelloid 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 non-metazoan 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.
  
  
  CONCLUSIONS
  Nearly half of foreign genes were acquired before the divergence of bdelloid families over 60 Mya. 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.
authors.affiliation: Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, SL5 7PY, UK.|Department of Animal and Plant Sciences, University of Sheffield, Alfred Denny Building, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Isobel
authors.initials: I
authors.lastname: Eyres
authors.affiliation: Department of Chemical Engineering and Biotechnology, University of Cambridge, New Museums Site, Pembroke Street, Cambridge, CB2 3RA, UK.
authors.forename: Chiara
authors.initials: C
authors.lastname: Boschetti
authors.affiliation: Department of Chemical Engineering and Biotechnology, University of Cambridge, New Museums Site, Pembroke Street, Cambridge, CB2 3RA, UK.
authors.forename: Alastair
authors.initials: A
authors.lastname: Crisp
authors.affiliation: Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, SL5 7PY, UK.
authors.forename: Thomas P
authors.initials: TP
authors.lastname: Smith
authors.affiliation: National Research Council, Institute of Ecosystem Study, Largo Tonolli 50, 28922, Verbania Pallanza, Italy.
authors.forename: Diego
authors.initials: D
authors.lastname: Fontaneto
authors.affiliation: Department of Chemical Engineering and Biotechnology, University of Cambridge, New Museums Site, Pembroke Street, Cambridge, CB2 3RA, UK.
authors.forename: Alan
authors.initials: A
authors.lastname: Tunnacliffe
authors.affiliation: Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, SL5 7PY, UK. t.barraclough@imperial.ac.uk.
authors.forename: Timothy G
authors.initials: TG
authors.lastname: Barraclough
mesh_terms: D000818:Animals; D003890:Desiccation; D017753:Ecosystem; D022761:Gene Transfer, Horizontal; D008969:Molecular Sequence Data; D010802:Phylogeny; D012403:Rotifera / Q000235:genetics*; D017422:Sequence Analysis, DNA; D013045:Species Specificity