Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals

doi:10.1073/pnas.0700531104

Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals

Oliver Piskurek and
Norihiro Okada*

Faculty of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B21 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan

Edited by Margaret G. Kidwell, University of Arizona, Tucson, AZ, and approved May 8, 2007 (received for review January 23, 2007)

Abstract

Poxviruses (Poxviridae) are a family of double-stranded DNA viruses with no RNA stage. Members of the genus Orthopoxvirus (OPV) are highly invasive and virulent. It was recently shown that the taterapox virus (TATV) from a West African rodent is the sister of camelpox virus and therefore belongs to the clade closest to the variola virus (VARV), the etiological agent of smallpox. Although these OPVs are among the most dreaded pathogens on Earth, our current knowledge of their genomes, their origins, and their possible hosts is still very limited. Here, we report the horizontal transfer of a retroposon (known only from reptilian genomes) to the TATV genome. After isolating and analyzing different subfamilies of short interspersed elements (SINEs) from lizards and snakes, we identified a highly poisonous snake (Echis ocellatus) from West Africa as the closest species from which the SINE sequence discovered in the TATV genome (TATV-SINE) was transferred to the virus. We discovered direct repeats derived from the virus flanking the TATV-SINE, and the absence of any snake-derived DNA flanking the SINE. These data provide strong evidence that the TATV-SINE was actually transferred within the snake to the viral genome by retrotransposition and not by any horizontal transfer at the DNA level. We propose that the snake is another host for TATV, suggesting that VARV-related epidemiologically relevant viruses may have derived from our cold-blooded ancestors and that poxviruses are possible vectors for horizontal transfer of retroposons from reptiles to mammals.

Footnotes

*To whom correspondence should be addressed. E-mail: nokada{at}bio.titech.ac.jp
Author contributions: O.P. designed research; O.P. performed research; O.P. analyzed data; and O.P. and N.O. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EF033459–EF033488 and EF101172–EF101210).
↵ † All Tatera species from Africa have recently been proposed to be distinct from the Asian Tatera indica and were therefore elevated to genus rank (31). The new genus is called Gerbilliscus.
This article contains supporting information online at www.pnas.org/cgi/content/full/0700531104/DC1.
↵ ‡ Although only T. kempi is shown in the electrophoresis, several other rodents were tested under these PCR conditions. However, the results were the same (data not shown).
Abbreviations:

EN,

endonuclease;

EOC,

Sauria SINE subfamily in advanced snakes isolated from Echis ocellatus;

LINE,

long interspersed element;

OPV,

Orthopoxvirus;

RT,

reverse transcriptase;

SINE,

short interspersed element;

TATV,

Taterapox virus;

TPRT,

target-primed reverse transcription;

VARV,

Variola virus.