Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Abstract

Horizontal gene transfer (HGT), or the transfer of genes between species, has been recognized recently as more pervasive than previously suspected. Here, we report evidence for an unprecedented degree of HGT into an animal genome, based on a draft genome of a tardigrade, Hypsibius dujardini. Tardigrades are microscopic eight-legged animals that are famous for their ability to survive extreme conditions. Genome sequencing, direct confirmation of physical linkage, and phylogenetic analysis revealed that a large fraction of the H. dujardini genome is derived from diverse bacteria as well as plants, fungi, and Archaea. We estimate that approximately one-sixth of tardigrade genes entered by HGT, nearly double the fraction found in the most extreme cases of HGT into animals known to date. Foreign genes have supplemented, expanded, and even replaced some metazoan gene families within the tardigrade genome. Our results demonstrate that an unexpectedly large fraction of an animal genome can be derived from foreign sources. We speculate that animals that can survive extremes may be particularly prone to acquiring foreign genes.

Reply to Bemm et al. and Arakawa: Identifying foreign genes in independent Hypsibius dujardini genome assemblies

“…The level of HGT that we infer remains higher than in most animals that have been tested (Fig. 1), although not as high a level as we had originally concluded (1).…”

“…This assembly was 252 Mb, larger than the 212.3-Mb assembly that we had used in our report (1), as pointed out correctly by others (5). The 212.3-Mb assembly used in our report is available at the link provided below.…”

“…Our report (1) describing the discovery of extensive horizontal gene transfer in a tardigrade genome has raised questions from other groups who were sequencing the Hypsibius dujardini genome in parallel or who have done new experiments and analyses since our report (2)(3)(4)(5). Bemm et al (2) now report filtering our data for likely contaminants, resulting in a new, prefiltered genome assembly.…”

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

“…Many species of Tardigrada can survive extreme conditions through cryptobiosis. In a recent paper [Boothby TC, et al (2015) Proc Natl Acad Sci USA 112(52):15976-15981], the authors concluded that the tardigrade Hypsibius dujardini had an unprecedented proportion (17%) of genes originating through functional horizontal gene transfer (fHGT) and speculated that fHGT was likely formative in the evolution of cryptobiosis. We independently sequenced the genome of H. dujardini.…”

“…Hypsibius dujardini (Doyère, 1840) is a limnetic tardigrade that is an emerging model for evolutionary developmental biology (4,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21). It is easily cultured in the laboratory, is largely see-through (aiding analyses of development and anatomy; SI Appendix, Fig.…”