| 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. |
| Source | BMC biology 13 (1) |
| Keywords | AdaptationBdelloid rotifersEvolutionHorizontal gene transferLateral gene transferMetazoans |
| Journal | BMC biology |
| Editor | BioMed Central,, [London], Regno Unito |
| Year | 2015 |
| Type | Articolo in rivista |
| DOI | 10.1186/s12915-015-0202-9 |
| Authors | Eyres, Isobel; Eyres, Isobel; Boschetti, Chiara; Crisp, Alastair; Smith, Thomas P.; Fontaneto, Diego; Tunnacliffe, Alan; Barraclough, Timothy G. |
| Text | 337738 2015 10.1186/s12915 015 0202 9 Scopus 2 s2.0 84946213308 ISI Web of Science WOS 000364118600001 Adaptation Bdelloid rotifers Evolution Horizontal gene transfer Lateral gene transfer Metazoans Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats Eyres, Isobel; Eyres, Isobel; Boschetti, Chiara; Crisp, Alastair; Smith, Thomas P.; Fontaneto, Diego; Tunnacliffe, Alan; Barraclough, Timothy G. Imperial College London; University of Cambridge; National Research Council; University of Sheffield 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. 13 Published version http //www.biomedcentral.com/1741 7007/13/90 eyres 2015_BmcBiol_Eyres_et_al.pdf Articolo in rivista BioMed Central, 1741 7007 BMC biology BMC biology BMC biology Biology BioMed Central biology diego.fontaneto FONTANETO DIEGO |
