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Journal of Virology, January 2008, p. 371-381, Vol. 82, No. 1
0022-538X/08/$08.00+0     doi:10.1128/JVI.01410-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Structure of the Acidianus Filamentous Virus 3 and Comparative Genomics of Related Archaeal Lipothrixviruses

Gisle Vestergaard,¹ Ricardo Aramayo,² Tamara Basta,³ Monika Häring,^3,4 Xu Peng,¹ Kim Brügger,¹ Lanming Chen,¹ Reinhard Rachel,⁴ Nicolas Boisset,² Roger A. Garrett,¹ and David Prangishvili^3*

Centre for Comparative Genomics and Danish Archaea Centre, Department of Molecular Biology, Biocenter, Copenhagen University, Ole Maaløes Vej 5, DK-2200 Copenhagen N, Denmark,¹ Institut de Minéralogie et de Physique des Milieux Condensés, Université Pierre et Marie Curie, IMPMC-UMR7590, Paris F-75005, France,² Molecular Biology of the Gene in Extremophiles Unit, Institut Pasteur, rue du Dr. Roux 25, 75724 Paris Cedex 15, France,³ Department of Microbiology, University of Regensburg, Universitätsst. 31, D-93053 Regensburg, Germany⁴

Received 28 June 2007/ Accepted 4 October 2007

Four novel filamentous viruses with double-stranded DNA genomes, namely, Acidianus filamentous virus 3 (AFV3), AFV6, AFV7, and AFV8, have been characterized from the hyperthermophilic archaeal genus Acidianus, and they are assigned to the Betalipothrixvirus genus of the family Lipothrixviridae. The structures of the approximately 2-µm-long virions are similar, and one of them, AFV3, was studied in detail. It consists of a cylindrical envelope containing globular subunits arranged in a helical formation that is unique for any known double-stranded DNA virus. The envelope is 3.1 nm thick and encases an inner core with two parallel rows of protein subunits arranged like a zipper. Each end of the virion is tapered and carries three short filaments. Two major structural proteins were identified as being common to all betalipothrixviruses. The viral genomes were sequenced and analyzed, and they reveal a high level of conservation in both gene content and gene order over large regions, with this similarity extending partly to the earlier described betalipothrixvirus Sulfolobus islandicus filamentous virus. A few predicted gene products of each virus, in addition to the structural proteins, could be assigned specific functions, including a putative helicase involved in Holliday junction branch migration, a nuclease, a protein phosphatase, transcriptional regulators, and glycosyltransferases. The AFV7 genome appears to have undergone intergenomic recombination with a large section of an AFV2-like viral genome, apparently resulting in phenotypic changes, as revealed by the presence of AFV2-like termini in the AFV7 virions. Shared features of the genomes include (i) large inverted terminal repeats exhibiting conserved, regularly spaced direct repeats; (ii) a highly conserved operon encoding the two major structural proteins; (iii) multiple overlapping open reading frames, which may be indicative of gene recoding; (iv) putative 12-bp genetic elements; and (v) partial gene sequences corresponding closely to spacer sequences of chromosomal repeat clusters.

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* Corresponding author. Mailing address: Institut Pasteur, rue du Dr. Roux 25, 75724 Paris Cedex 15, France. Phone: 33(0)1 44 38 91 19. Fax: 33(0)1 45 68 88 34. E-mail: prangish{at}pasteur.fr

Published ahead of print on 17 October 2007.

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Journal of Virology, January 2008, p. 371-381, Vol. 82, No. 1
0022-538X/08/$08.00+0     doi:10.1128/JVI.01410-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

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