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

Thomas C. Boothby; Jennifer R. Tenlen; Frank W. Smith; Jeremy R. Wang; Kiera A. Patanella; Erin Osborne Nishimura; Sophia C. Tintori; Qing Li; Corbin D. Jones; Mark Yandell; David N. Messina; Jarret Glasscock; Bob Goldstein

doi:10.1073/pnas.1510461112

Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved September 28, 2015 (received for review May 28, 2015)

Significance

Despite fascinating scientists for over 200 years, little at the molecular level is known about tardigrades, microscopic animals resistant to extreme stresses. We present the genome of a tardigrade. Approximately one-sixth of the genes in the tardigrade genome were found to have been acquired through horizontal transfer, a proportion nearly double the proportion of previous known cases of extreme horizontal gene transfer (HGT) in animals. Foreign genes have impacted the composition of the tardigrade genome: supplementing, expanding, and replacing endogenous gene families, including those families implicated in stress tolerance. Our results extend recent findings that HGT is more prevalent in animals than previously suspected, and they suggest that organisms that survive extreme stresses might be predisposed to acquiring foreign genes.

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.

Footnotes

↵¹To whom correspondence should be addressed. Email: tboothby{at}gmail.com.
↵²Present address: Department of Biology, Seattle Pacific University, Seattle, WA 98119.

Author contributions: T.C.B. and B.G. designed research; T.C.B., J.R.T., K.A.P., E.O.N., S.C.T., D.N.M., and J.G. performed research; T.C.B., F.W.S., J.R.W., Q.L., C.D.J., and M.Y. analyzed data; J.R.T., E.O.N., and S.C.T. isolated material for sequencing; J.R.W. and C.D.J. performed Pacific Biosciences sequencing and assembly; Q.L. and M.Y. performed genome annotation; D.N.M. and J.G. performed Illumina sequencing and assembly; and T.C.B. and B.G. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: This Whole Genome Shotgun project has been deposited in the DDBJ/EMBL/GenBank database (accession no. LMYF00000000). The version described in this paper is version LMYF01000000.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1510461112/-/DCSupplemental.