Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus - PubMed (original) (raw)

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

Ellen J Pritham et al. Proc Natl Acad Sci U S A. 2007.

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 approximately 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 (approximately 15,000 and > 100,000 copies, respectively) and make up at least approximately 3% of the M. lucifugus genome. Sequence divergence and cross-species analyses indicate that both HeliBat families have amplified within the last approximately 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 approximately 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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Terminal sequence features of HeliBat elements and other Helitrons. The 5′ and 3′ terminal sequences characteristic of Helitrons are shaded in black, and the 3′ palindromic motifs are underlined. The flanking A and T host nucleotides are in lowercase. Ml, M. lucifugus; Ce, C. elegans; Ag, Anopheles gambiae; Os, Oryza sativa; At, A. thaliana.

Fig. 2.

Fig. 2.

Genetic organization and predicted functional protein domains of HeliBat1. (Top) A schematic representation of the genetic organization of HeliBat1 and domain structure of the putative encoded protein. ZF, zinc-finger-like motifs; Rep, RC replication initiator motif; Helicase, region similar to SF1 superfamily of DNA helicases. (Middle) An alignment of the REP motif of HeliBat1, representative Helitrons from seven other species [abbreviations as in Fig. 1, plus Sp, Strongylocentrotus purpuratus; Cg, Chaetomium globosum (a fungus); Dr, _Danio rerio_] and several RC viruses and plasmids (SVTS, Spiroplasma plectrovirus; Rep_SC, Streptomyces cyaneus plasmid; Rep_BB, Bacillus borstelensis plasmid; Rep_AA, Actinobacillus actinomycetemcomitans plasmid; TRAA_RHISN, Rhizobium sp.; NGR234Pf3, Pseudomonas aeruginosa bacteriophage). The positions of the two histidines and two tyrosines known to be critical for catalytic activity of the RC elements are highlighted above the alignment. (Bottom) An alignment of the seven conserved motifs of SF1 superfamily DNA helicases from yeast (P07271), baculovirus (T30397), bacteria (P55418), and T4 phage (P32270) with the corresponding regions of HeliBat1 and other Helitron proteins.

Fig. 3.

Fig. 3.

Neighbor-joining phylogenetic analysis of HeliBat1 and other Helitron and _Helitron_-like proteins. The accession numbers for the Helitron putative proteins are preceded by the species name abbreviated as in Fig. 1 and 2. The Helitron2 and Helentron1 proteins are from refs. and . The midpoint rooting option was used, and bootstrap scores > 50% were retained. Ag, Anopheles gambiae; Bo, Brassica oleracea; Mt, Medicago trunculata.

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