Viruses of Hyperthermophilic Crenarchaea

Review TRENDS in Microbiology Vol.13 No.11 November 2005 Viruses of hyperthermophilic Crenarchaea David Prangishvili1 and Roger A. Garrett2 1Molecular Biology of the Gene in Extremophiles Unit, Institut Pasteur, rue Dr. Roux 25, 75724 Paris Cedex 15, France 2Danish Archaea Centre, Institute of Molecular Biology and Physiology, Copenhagen University, Sølvgade 83H, DK-1307 Copenhagen K, Denmark Since the discovery of the Archaea – the third domain of one minor geothermal pool. For Figure 1 and Figure 3, the life – by Woese and colleagues in 1977, the subsequent host range constitutes a few closely related strains of the developments in molecular and cell biology, and also crenarchaeal genus Acidianus, whereas for Figure 2 genomics, have strongly reinforced the view that the host range spectrum is broader and includes repre- archaea and eukarya co-evolved, separately from bac- sentatives of the crenarchaeal genera Thermosphaera, teria, over a long time. However, when one examines Desulfurococcus, Thermophilum and Pyrobaculum the archaeal viruses, the picture appears complex. Most (M. Ha¨ring and D. Prangishvili, unpublished data). Of viruses that are known to infect members of the the particle types observed in the three enrichment kingdom Euryarchaeota resemble bacterial viruses, cultures, w40% were shown to be infectious virions and whereas those associated with the kingdom Crenarch- could be isolated and cultured [Figure 1b (virus AFV1); aeota show little resemblance to either bacterial or Figure 2c,d (virus PSV, indicated by arrows); Figure 3a eukaryal viruses. This review summarizes our current (virus ABV), 3b (virus ATV), 3c (virus ARV1), 3d (virus knowledge of this group of exceptional and highly AFV2), 3d (virus AFV3)]. diverse archaeal viruses. To date, w25 crenarchaeal viruses have been isolated from hot terrestrial habitats and characterized; these were found to infect members of the genera Sulfolobus, Acidianus, Pyrobaculum and Thermoproteus. Many of Morphological diversity these viruses have been classified into seven new families Early studies on viruses from the domain Archaea on the basis of their morphotypes and the properties of concentrated on those infecting extremely halophilic and their double-stranded (ds) DNA genomes (Table 1). Four of methanogenic members of the kingdom Euryarchaeota. the families have already been approved by the Inter- Most of these viruses are similar to head-tail bacterio- national Committee of Taxonomy of Viruses. phages in morphotype and genome organization and were assigned to the families Myoviridae and Siphoviridae (reviewed in Ref. [1]). Later, the development of methods Morphotypes unique amongst viruses for cultivating aerobic and anaerobic hyperthermophiles Virions of the Fuselloviridae family are spindle-shaped led to the discovery of viruses infecting members of the with a single short tail that carries fibers, positioned at other major archaeal kingdom, the Crenarchaeota. The only one of the two similar poles, which facilitate the morphotypes of the first of these viruses to be character- attachment of virions to the host membrane. The ized were exceptional and quite unexpected (reviewed in unclassified STSV1 virus is much larger than the [2]). Subsequent screening for crenarchaeal viruses in fuselloviruses but exhibits a similar form [7].The different geographical locations, including geothermally structure of the inner core of the enveloped virions, heated springs (O808C), reinforced and extended the which apparently generates the unusual shape, is earlier results [3–5]. These studies revealed that cre- unknown. A similar uncertainty exists concerning the narchaeal viruses exhibit highly diverse morphotypes inner-core structure of the enveloped, droplet-shaped and, although some shapes (e.g. the spherical form of PSV virion of SNDV, the sole member of the Guttaviridae.A and STIV [4,6]) are common for viruses, others are large number of densely packed thin filaments protrude extraordinary. Examples of morphotypes observed in the from the pointed end of the virion and these are likely to enrichment cultures from these habitats are illustrated in participate in cellular adsorption. SNDV is the least Figures 1–3. The most abundant particles in the enrich- studied of the isolated crenarchaeal viruses [8] and, ments exhibit linear morphotypes, which are either unfortunately, a host strain in which it could be replicated flexible or rigid (Figure 1a,b,e–g; Figure 2a,b,d; stably has not been found; therefore, the virus no longer Figure 3c–e), as well as spindle-shaped particles with exists in laboratory collections. tails of different size and form (Figure 1d,h,j; Figure 2e). The enveloped virion of ABV, the sole member of the Each figure includes virions or virion-like particles from Ampullaviridae, resembles a bottle (Figure 3a), the Corresponding author: Garrett, R.A. ([email protected]). narrow end of which is likely to be involved in cellular Available online 8 September 2005 adsorption and in channeling of viral DNA into the host www.sciencedirect.com 0966-842X/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tim.2005.08.013 536 Review TRENDS in Microbiology Vol.13 No.11 November 2005 Figure 1. Transmission electron micrographs of a variety of viruses and virus-like particles observed in a single enrichment culture established from of a sample taken from a geothermally heated, hot acidic spring (858C, pH 1.5–2.0) in Yellowstone National Park, USA. (a) A rod-shaped helical particle; inset: enlarged terminus; (b) a filamentous particle of the virus AFV1; inset: enlarged terminus, (c) a particle with ellipsoid body and two helical tails; (d) spindle-shaped particles; (e) short rod-shaped helical particles; (f) a filamentous particle with bulbous termini, both shown enlarged in the insets; (g) a filamentous particle with rounded ends, which are shown enlarged in the insets; (h) a spindle-shaped particle with a helical tail, enlarged in the inset; (i) four zipper-shaped particles; (j) four pleomorphic particles with arrow-shaped heads and tails of different length. Samples were negatively stained with 2% uranyl acetate. Bars: 200 nm (100 nm for insets). Modified with permission from Ref. [4]. cell [5]. The broad end exhibits 20 thin filaments, which genomic properties and their possible replication strat- are inserted into a disk and interconnected at the base. egies (see subsequent sections). The terminal structures at The filaments do not seem to be involved in cellular each end of a given lipothrixvirus are identical, as judged adsorption and their function remains unclear but from electron microscopy studies, although those of TTV1 intriguing. ATV, the only member of the Bicaudaviridae, have not been analyzed in detail [10]. For SIFV, the body contains a lemon-shaped central structure with elongated tapers and ends in mop-like structures [11], AFV1 exhibits tails protruding from both pointed ends (Figure 3b). claw-like terminal structures, connected to the virion body Members of two viral families exhibit morphotypes by appendages [12], and AFV2 carries a complex collar similar to those of eukaryal viruses with single-stranded with two sets of filaments, resembling a bottle brush with (ss) RNA genomes. Thus, the rod-shaped non-enveloped a solid round cap at each end [13]. These terminal virions of the Rudiviridae (Figure 3c) resemble ssRNA structures are implicated in cellular adsorption for each viruses of vascular plants, with a body consisting of the of the lipothrixviruses and both termini seem capable of viral genome assembled with multiple copies of a single attaching to cellular receptors [12]. Most viruses adsorb DNA-binding protein [9]. However, in contrast to tobamo- directly to host cells and the mop-like terminal structures viruses, the rudiviruses have specific terminal structures, of SIFV have been shown to unfold like spiders legs before consisting of three tail fibers protruding from each end, attachment to cell membranes [11]. An exception is AFV1, which are required for adsorption on the host cell surface. in which the claw-like ends clamp onto host pili [12]. Virions of the family Globuloviridae are spherical and The arrangement of the virion cores, which are encased by carry an envelope (Figure 2d) that encases a superhelical envelopes, differs between the lipothrixviral genera although nucleoprotein core. This structure resembles that of all carry linear dsDNA genomes. The cores of TTV1 and AFV1 ssRNA viruses of the Paramyxoviridae, which infect are helical and that of TTV1 was shown to contain equimolar vertebrates. amounts of two DNA-binding proteins [10]. The arrangement Members of the Lipothrixviridae have filamentous, of the SIFV core, with linear DNAwound around a zipper-like enveloped virions (Figure 1b and Figure 3d,e) and have array of a putative heterotetramer containing two proteins, been classified into four different genera (Table 1) on the resembles nucleosomes [11]. By contrast, no regular struc- basis of differences in core, terminal structures and ture was detected in the core of AFV2 [13]. www.sciencedirect.com Review TRENDS in Microbiology Vol.13 No.11 November 2005 537 Figure 2. Transmission electron micrographs of a variety of viruses and virus-like particles observed in a single enrichment culture established from a sample taken from a geothermally heated, hot spring (75–938C, pH 6.5) in Yellowstone National Park, USA. (a,b) Two types of rod-shaped particles with different termini, shown enlarged in insets;

Load more