Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus

Department of Biology, University of Texas, Arlington, TX 76019

Edited by Susan R. Wessler, University of Georgia, Athens, GA, and approved December 18, 2006 (received for review October 28, 2006)

Abstract

Rolling-circle (RC) transposons, or Helitrons, are a newly recognized group of eukaryotic transposable elements abundant in the genomes of plants, invertebrates, and zebrafish. We provide evidence for the colonization of a mammalian genome by Helitrons, which has not been reported previously. We identified and characterized two families of Helitrons in the little brown bat Myotis lucifugus. The consensus sequence for the first family, HeliBat1, displays the hallmarks of an autonomous Helitron, including coding capacity for an ≈1,500-aa protein with an RC replication motif and a region related to the SF1 superfamily of DNA helicases. The HeliBatN1 family is a nonautonomous Helitron family that is only distantly related to HeliBat1. The two HeliBat families have attained high copy numbers (≈15,000 and > 100,000 copies, respectively) and make up at least ≈3% of the M. lucifugus genome. Sequence divergence and cross-species analyses indicate that both HeliBat families have amplified within the last ≈30–36 million years and are restricted to the lineage of vesper bats. We could not detect the presence of Helitrons in any other order of placental mammals, despite the broad representation of these taxa in the databases. We describe an instance of HeliBat-mediated transduction of a host gene fragment that was subsequently dispersed in ≈1,000 copies throughout the M. lucifugus genome. Given the demonstrated propensity of RC transposons to mediate the duplication and shuffling of host genes in bacteria and maize, it is tempting to speculate that the massive amplification of Helitrons in vesper bats has influenced the evolutionary trajectory of these mammals.

Footnotes

*To whom correspondence may be addressed. E-mail: pritham{at}uta.edu or cedric{at}uta.edu
Author contributions: E.J.P. and C.F. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS direct submission.
Data desposition: Consensus sequences for the HeliBat families described in this study were deposited in Repbase, www.girinst.org/repbase (accession numbers and coordinates of the individual sequences used to reconstruct the consensus are listed in SI Table 1).
This article contains supporting information online at www.pnas.org/cgi/content/full/0609601104/DC1.
Abbreviations:

MYA,

million years ago;

RC,

rolling circle;

TE,

transposable element;

WGS,

whole genome shotgun sequences.