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Journal of Virology, September 2002, p. 8920-8930, Vol. 76, No. 17
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.17.8920-8930.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Molecular Analysis of Three Ljungan Virus Isolates Reveals a New, Close-to-Root Lineage of the Picornaviridae with a Cluster of Two Unrelated 2A Proteins{dagger}

Susanne Johansson,1 Bo Niklasson,2 Jacob Maizel,3 Alexander E. Gorbalenya,4* and A. Michael Lindberg1*

Department of Chemistry and Biomedical Sciences, University of Kalmar, S-391 82 Kalmar,1 Nya Apodemus, S-114 53 Stockholm, Sweden,2 Laboratory of Experimental and Computational Biology, National Cancer Institute,3 Advanced Biomedical Computing Center, SAIC/National Cancer Institute-Frederick Cancer Research and Development Center, Frederick, Maryland 217024

Received 27 December 2001/ Accepted 3 June 2002

Ljungan virus (LV) is a suspected human pathogen recently isolated from bank voles (Clethrionomys glareolus). In the present study, it is revealed through comparative sequence analysis that three newly determined Swedish LV genomes are closely related and possess a deviant picornavirus-like organization: 5' untranslated region-VP0-VP3-VP1-2A1-2A2-2B-2C-3A-3B-3C-3D-3' untranslated region. The LV genomes and the polyproteins encoded by them exhibit several exceptional features, such as the absence of a predicted maturation cleavage of VP0, a conserved sequence determinant in VP0 that is typically found in VP1 of other picornaviruses, and a cluster of two unrelated 2A proteins. The 2A1 protein is related to the 2A protein of cardio-, erbo-, tescho-, and aphthoviruses, and the 2A2 protein is related to the 2A protein of parechoviruses, kobuviruses, and avian encephalomyelitis virus. The unprecedented association of two structurally different 2A proteins is a feature never previously observed among picornaviruses and implies that their functions are not mutually exclusive. Secondary polyprotein processing of the LV polyprotein is mediated by proteinase 3C (3Cpro) possessing canonical affinity to Glu and Gln at the P1 position and small amino acid residues at the P1' position. In addition, LV 3Cpro appears to have unique substrate specificity to Asn, Gln, and Asp and to bulky hydrophobic residues at the P2 and P4 positions, respectively. Phylogenetic analysis suggests that LVs form a separate division, which, together with the Parechovirus genus, has branched off the picornavirus tree most closely to its root. The presence of two 2A proteins indicates that some contemporary picornaviruses with a single 2A may have evolved from the ancestral multi-2A picornavirus.

* Corresponding author. Mailing address for A. Michael Lindberg: Department of Chemistry and Biomedical Sciences, University of Kalmar, S-391 82 Kalmar, Sweden. Phone: 46 480 446240. Fax: 46 480 446262. E-mail: michael.lindberg{at}hik.se. Present address for Alexander E. Gorbalenya: Department of Medical Microbiology, Center of Infectious Diseases, Leiden University Medical Center, L04-36, P.O. Box 9600, 2300 RC Leiden, The Netherlands. Phone: 31 71 5261652. Fax: 31 71 5266761. E-mail: a.e.gorbalenya{at}lumc.nl.

{dagger} This paper is dedicated to the memory of Don Summers, a friend and colleague, who will be greatly missed.

Journal of Virology, September 2002, p. 8920-8930, Vol. 76, No. 17
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.17.8920-8930.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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