Trends in Microbiology
Viruses of hyperthermophilic Crenarchaea
Section snippets
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.
References (35)
Haloarchaeal viruses: how diverse are they?
Res. Microbiol.
(2003)Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic archaea
FEMS Microbiol. Rev.
(1996)SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus
Virology
(2000)A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus
Virology
(2000)AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus
Virology
(2003)Morphology and genome organization of the virus PSV of the hyperthermophilic archaea genera Pyrobaculum and Thermoproteus: A novel virus family, the Globuloviridae
Virology
(2004)Archaebacterial viruses
Adv. Virus Res.
(1988)ARV1, a novel rudivirus infecting the hyperthermophilic genus Acidianus
Virology
(2005)The linear genome of the archaeal virus SIRV1 has features in common with genomes of eukaryal viruses
Virology
(2001)Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses
Virology
(2001)
Holliday junction resolving enzymes of archaeal viruses SIRV1 and SIRV2
J. Mol. Biol.
Transcription in archaea
Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae
Virology
Biological and genetic relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2
Res. Microbiol.
Viruses from extreme thermal environments
Proc. Natl. Acad. Sci. U. S. A.
Remarkable morphological diversity of viruses and virus-like particles in hot terrestial environments
Arch. Virol.
Virusal diversity in hot springs of Pozzuoli, Italy, and characterisation of a unique archaeal virus Acidianus bottle-shaped virus, from a new viral family, the Ampullaviridae
J. Virol.
Cited by (71)
Bacteriophage P23-77 capsid protein structures reveal the archetype of an ancient branch from a major virus lineage
2013, StructureCitation Excerpt :Extreme environments such as the hot springs inhabited by the host of P23-77, bacterial genus Thermus (optimal growth temperature from 65 to 75°C; Beffa et al., 1996), are dominated by a few organisms (Hacene et al., 2004; Oren, 2002; Skirnisdottir et al., 2000). However, viral communities in such environments are abundant and show a remarkable diversity of morphotypes that are not found in moderate habitats (Prangishvili, 2003; Prangishvili and Garrett, 2005; Rice et al., 2001; Sime-Ngando et al., 2011). Extreme environments appear to represent stable, nonoverlapping ecological niches in which close communities of a few highly adapted species thrive, changing extremely slowly (Drake, 2009; Friedman et al., 2004).
Functional biology and biotechnology of thermophilic viruses
2023, Essays in BiochemistryIsolation of archaeal viruses with lipid membrane from Tengchong acidic hot springs
2023, Frontiers in MicrobiologySurface resistance to SSVs and SIRVs in pilin deletions of Sulfolobus islandicus
2020, Molecular MicrobiologyArchaeal viruses and their interactions with CRISPR-cas systems
2020, Biocommunication of Phages