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Journal of Bacteriology, October 2008, p. 6837-6845, Vol. 190, No. 20
0021-9193/08/$08.00+0     doi:10.1128/JB.00795-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Stygiolobus Rod-Shaped Virus and the Interplay of Crenarchaeal Rudiviruses with the CRISPR Antiviral System{triangledown} ,{dagger}

Gisle Vestergaard,1 Shiraz A. Shah,1 Ariane Bize,2 Werner Reitberger,3 Monika Reuter,3 Hien Phan,1 Ariane Briegel,4 Reinhard Rachel,3 Roger A. Garrett,1 and David Prangishvili2*

Danish Archaea Centre and Centre for Comparative Genomics, Department of Biology, Copenhagen University, Ole Maaløes Vej 5, DK-2200 Copenhagen N, Denmark,1 Molecular Biology of the Gene in Extremophiles Unit, Institut Pasteur, rue Dr. Roux 25, 75724 Paris Cedex 15, France,2 Department of Microbiology, University of Regensburg, Universitätsstrasse 31, D-93053 Regensburg, Germany,3 Max-Planck-Institut of Biochemistry, Molecular Structural Biology, Am Klopferspitz 21, D-82152 Martinsried, Germany4

Received 6 June 2008/ Accepted 11 August 2008

A newly characterized archaeal rudivirus Stygiolobus rod-shaped virus (SRV), which infects a hyperthermophilic Stygiolobus species, was isolated from a hot spring in the Azores, Portugal. Its virions are rod-shaped, 702 (± 50) by 22 (± 3) nm in size, and nonenveloped and carry three tail fibers at each terminus. The linear double-stranded DNA genome contains 28,096 bp and an inverted terminal repeat of 1,030 bp. The SRV shows morphological and genomic similarities to the other characterized rudiviruses Sulfolobus rod-shaped virus 1 (SIRV1), SIRV2, and Acidianus rod-shaped virus 1, isolated from hot acidic springs of Iceland and Italy. The single major rudiviral structural protein is shown to generate long tubular structures in vitro of similar dimensions to those of the virion, and we estimate that the virion constitutes a single, superhelical, double-stranded DNA embedded into such a protein structure. Three additional minor conserved structural proteins are also identified. Ubiquitous rudiviral proteins with assigned functions include glycosyl transferases and a S-adenosylmethionine-dependent methyltransferase, as well as a Holliday junction resolvase, a transcriptionally coupled helicase and nuclease implicated in DNA replication. Analysis of matches between known crenarchaeal chromosomal CRISPR spacer sequences, implicated in a viral defense system, and rudiviral genomes revealed that about 10% of the 3,042 unique acidothermophile spacers yield significant matches to rudiviral genomes, with a bias to highly conserved protein genes, consistent with the widespread presence of rudiviruses in hot acidophilic environments. We propose that the 12-bp indels which are commonly found in conserved rudiviral protein genes may be generated as a reaction to the presence of the host CRISPR defense system.

* Corresponding author. Mailing address: Molecular Biology of the Gene in Extremophiles Unit, Institut Pasteur, rue Dr. Roux 25, 75724 Paris Cedex 15, France. Phone: 33-(0)144-38-9119. Fax: 33-(0)145-68-8834. E-mail: prangish{at}pasteur.fr

{triangledown} Published ahead of print on 22 August 2008.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, October 2008, p. 6837-6845, Vol. 190, No. 20
0021-9193/08/$08.00+0     doi:10.1128/JB.00795-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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