A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors

Xin-Cheng Qin; Mang Shi; Jun-Hua Tian; Xian-Dan Lin; Dong-Ya Gao; Jin-Rong He; Jian-Bo Wang; Ci-Xiu Li; Yan-Jun Kang; Bin Yu; Dun-Jin Zhou; Jianguo Xu; Alexander Plyusnin; Edward C. Holmes; Yong-Zhen Zhang

doi:10.1073/pnas.1324194111

New Research In

Edited by Peter Palese, Icahn School of Medicine at Mount Sinai, New York, NY, and approved March 27, 2014 (received for review December 30, 2013)

Significance

RNA viruses can contain a single (unsegmented) or multiple (segmented) genomic molecules. However, the evolutionary connection between these two fundamentally different forms of genome organization is unclear. We discovered a previously unidentified segmented RNA virus of ticks that, uniquely, contained two segments derived from an unsegmented flavivirus, as well as two highly divergent segments of unknown origin. In addition, copies of this virus were present in a nematode (dog roundworm). Collectively, these results demonstrate the remarkable diversity of viral genome structures as well as a previously unidentified evolutionary link between unsegmented and segmented viruses.

Abstract

Although segmented and unsegmented RNA viruses are commonplace, the evolutionary links between these two very different forms of genome organization are unclear. We report the discovery and characterization of a tick-borne virus—Jingmen tick virus (JMTV)—that reveals an unexpected connection between segmented and unsegmented RNA viruses. The JMTV genome comprises four segments, two of which are related to the nonstructural protein genes of the genus Flavivirus (family Flaviviridae), whereas the remaining segments are unique to this virus, have no known homologs, and contain a number of features indicative of structural protein genes. Remarkably, homology searching revealed that sequences related to JMTV were present in the cDNA library from Toxocara canis (dog roundworm; Nematoda), and that shared strong sequence and structural resemblances. Epidemiological studies showed that JMTV is distributed in tick populations across China, especially Rhipicephalus and Haemaphysalis spp., and experiences frequent host-switching and genomic reassortment. To our knowledge, JMTV is the first example of a segmented RNA virus with a genome derived in part from unsegmented viral ancestors.

Footnotes

↵¹X.-C.Q., M.S., J.-H.T., and X.-D.L. contributed equally to this work.
↵²To whom correspondence should be addressed. E-mail: zhangyongzhen{at}icdc.cn.

Author contributions: X.-C.Q., M.S., and Y.-Z.Z. designed research; X.-C.Q., M.S., J.-H.T., X.-D.L., D.-Y.G., J.-R.H., C.-X.L., and Y.-J.K. performed research; J.-H.T., X.-D.L., J.-B.W., B.Y., D.-J.Z., and J.X. contributed new reagents/analytic tools; X.-C.Q., M.S., J.X., A.P., E.C.H., and Y.-Z.Z. analyzed data; and M.S., A.P., E.C.H., and Y.-Z.Z. 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. KJ001547–KJ001634).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1324194111/-/DCSupplemental.

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