Trends in Microbiology
Volume 13, Issue 11, November 2005, Pages 535-542
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Viruses of hyperthermophilic Crenarchaea

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Since the discovery of the Archaea – the third domain of life – by Woese and colleagues in 1977, the subsequent developments in molecular and cell biology, and also genomics, have strongly reinforced the view that archaea and eukarya co-evolved, separately from bacteria, over a long time. However, when one examines the archaeal viruses, the picture appears complex. Most viruses that are known to infect members of the kingdom Euryarchaeota resemble bacterial viruses, whereas those associated with the kingdom Crenarchaeota show little resemblance to either bacterial or eukaryal viruses. This review summarizes our current knowledge of this group of exceptional and highly diverse archaeal viruses.

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Morphological diversity

Early studies on viruses from the domain Archaea concentrated on those infecting extremely halophilic and methanogenic members of the kingdom Euryarchaeota. Most of these viruses are similar to head-tail bacteriophages in morphotype and genome organization and were assigned to the families Myoviridae and Siphoviridae (reviewed in Ref. [1]). Later, the development of methods for cultivating aerobic and anaerobic hyperthermophiles led to the discovery of viruses infecting members of the other

Morphotypes unique amongst viruses

Virions of the Fuselloviridae family are spindle-shaped with a single short tail that carries fibers, positioned at only one of the two similar poles, which facilitate the attachment of virions to the host membrane. The unclassified STSV1 virus is much larger than the fuselloviruses but exhibits a similar form [7]. The structure of the inner core of the enveloped virions, which apparently generates the unusual shape, is unknown. A similar uncertainty exists concerning the inner-core structure

Virion components

The number of the major protein components present in the virions varies from 1–2 for fuselloviruses and rudiviruses to 11 proteins for the bicaudavirus ATV. N-terminal sequences have been determined for many of the major structural proteins and correlated with gene sequences. Some have been expressed and studied. For example, the 88.7-kDa protein encoded by ATV is rich in coiled-coil motifs and can generate structures that resemble intermediate filaments, which contribute to the elongated

Virus–host interactions

Hosts of all the cultured crenarchaeal viruses are members of the hyperthermophilic genera Sulfolobus, Acidianus, Thermoproteus and Pyrobaculum. The first two genera comprise extreme acidophiles, whereas members of the last two genera are all neutrophiles and obligate anaerobes. Infectivity of Thermoproteus and Pyrobaculum with viruses is unaffected by exposure to oxygen. For all of the hosts that grow optimally at 80°C or above, viral infection occurs most effectively at the optimal growth

Genome structure

The uniqueness and diversity of the viral morphotypes is reflected in their genomic properties. Each of the crenarchaeal viruses investigated so far carries a dsDNA genome. The circular genomes of the fuselloviruses, bicaudavirus ATV and STSV1 occur in the size range 15–75 kb (Table 1). All known rudiviruses, lipothrixviruses and globuloviruses contain linear genomes falling in the smaller size range 25–45 kb and some of them carry large inverted terminal repeats (ITR). Whether any of these

DNA replication

Genomic replication mechanisms have not been studied experimentally for any crenarchaeal viruses and they remain largely unknown, as do the protein components, host- or viral-encoded, which facilitate these processes. Nevertheless, the viral genome organizations and gene contents provide some clues. For example, the large circular genome of STSV1 exhibits a single putative origin of replication containing multiple, imperfect, A+T-rich repeats [7]. Moreover, the diverse structures of the linear

Transcription

Although studies on transcription of the fusellovirus SSV1 were crucial for our seminal understanding of mechanisms of transcriptional regulation in archaea [27], these studies examined the induction of viral replication in lysogens, rather than the infection cycle. Recently, the first detailed analysis of transcription over the complete replication cycle was performed on rudiviruses [28]. In vivo studies demonstrated a rather simple and ordered transcriptional pattern for both SIRV1 and SIRV2

Antisense RNAs

One haloarchaeal virus øH1 produces an antisense RNA, which generates a ∼150 bp RNA–RNA hybrid that is processed by a ss/ds-specific RNase in vivo [30]. Apart from an intron contained within a tRNALys encoded in the AFV2 genome [13], no untranslated RNAs have been found encoded in the crenarchaeal viral genomes. However, numerous putative antisense RNAs have been detected in Sulfolobus cells some of which might be involved in regulation of transposase activity [31] and some of the viruses carry

Genome variation

Different viruses show different degrees of genome stability. Sequencing of clone libraries of some genomes, including those of the rudiviruses SIRV2 and ARV1, showed no evidence of sequence heterogeneities even in genomic regions where the clone sequence coverage was 10–15-fold. Other genomes show local regions with a few point mutations or the odd duplication. For example, PSV clones revealed 34 point mutations, one-third of which were concentrated within one short intergenic region, and one

Exciting challenges

Double-stranded DNA viruses that infect the Crenarchaeota show no clear similarities in their morphologies and genomic properties to either bacterial or eukaryal viruses, nor do they resemble viruses of the Euryarchaeota. Moreover, failure to detect homologues for most of their genes in public databases suggests that they employ novel biochemical mechanisms for viral functions, which can now be studied in detail (see Box 1).

Thus, the replication mechanisms for the crenarchaeal viruses remain

Acknowledgements

We are grateful to Gisle Vestergaard, Monika Häring, Kim Brügger, Xu Peng, Alexandra Kessler, Reinhard Rachel and Qunxin She for their help and discussions and to Guennadi Sezonov for help in preparing the figures. We dedicate this review to the memory of the late Wolfram Zillig who pioneered work on crenarchaeal viruses.

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