Large Tailed Spindle Viruses of Archaea: a New Way of Doing Viral Business

We provide here, for the first time, insights into the initial infection stages of a large spindle-shaped archaeal virus and explore the following life cycle events. Our observations suggest that Sulfolobus monocaudavirus 1 (SMV1) exhibits a high adsorption rate and that virions adsorb to the host cells via three distinct attachment modes: nosecone association, body association, and body/tail association. In the body/tail association mode, the entire virion, including the tail(s), aligns to the host cell surface and the main body is greatly flattened, suggesting a possible fusion entry mechanism. Upon infection, the intracellular replication cycle lasts about 8 h, at which point the virions are released as spindle-shaped tailless particles. Replication of the virus retarded host growth but did not cause lysis of the host cells. Once released from the host and at temperatures resembling that of its natural habitat, SMV1 starts developing one or two tails. This exceptional property of undergoing a major morphological development outside, and independently of, the host cell has been reported only once before for the related Acidianus two-tailed virus. Here, we show that SMV1 can develop tails of more than 900 nm in length, more than quadrupling the total virion length. IMPORTANCE Very little is known about the initial life cycle stages of viruses infecting hosts of the third domain of life,Archaea. This work describes the first example of an archaeal virus employing three distinct association modes. The virus under study, Sulfolobus monocaudavirus 1, is a representative of the large spindle-shaped viruses that are frequently found in acidic hot springs. The results described here will add valuable knowledge about Archaea, the least studied domain in the virology field.A rchaeal viruses constitute an integral part of the virosphere, and they are a ubiquitous feature of archaeal existence. Many Archaea are recognized as extremophiles, inhabiting extreme environments such as hot springs and solar salterns in high abundance (1, 2). Thus, viruses infecting extremophilic Archaea can be considered key players in the complex population dynamics in these environments. Through host infection, viruses can influence microbial diversity by introducing genetic variation, affect host cell physiology, and directly kill their hosts by cell lysis (3, 4). However, we have only a rudimentary understanding of archaeal virus-host interactions. Much of the limited knowledge that we do have comes from studying the virus-host interplay in Sulfolobales species. Of the about 100 isolated archaeal viruses, more than 30% infect hyperthermophilic Sulfolobales hosts (5-7). Among these viruses, distinct characteristics are found: unique bottle, droplet, and spindle shapes; extracellular virion development; and unique proteins with unknown functions (8). These distinctive characteristics are likely to influence the interplay with their hosts and give rise to unique life cycle traits. This has proven true for the rodshaped Sulfolobus virus ...

Section: Very Little Is Known About the Initial Life Cycle Stages Of mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Life Cycle Characterization of Sulfolobus Monocaudavirus 1, an Extremophilic Spindle-Shaped Virus with Extracellular Tail Development

Uldahl

Jensen

Bhoobalan-Chitty

et al. 2016

“…The first group includes members of the Bicaudaviridae family and several currently unclassified viruses. Viruses of this group have large spindle-shaped virions with one or two long tails and contain circular double-stranded DNA (dsDNA) genomes of ϳ70 kb (11,25). In the case of Acidianus two-tailed virus (ATV), the type species of the Bicaudaviridae family, the two tails develop following …”

mentioning

confidence: 99%

Sulfolobus Spindle-Shaped Virus 1 Contains Glycosylated Capsid Proteins, a Cellular Chromatin Protein, and Host-Derived Lipids

Quemin

Pietilä

Oksanen

et al. 2015

Geothermal and hypersaline environments are rich in virus-like particles, among which spindle-shaped morphotypes dominate. Currently, viruses with spindle-or lemon-shaped virions are exclusive to Archaea and belong to two distinct viral families. The larger of the two families, the Fuselloviridae, comprises tail-less, spindle-shaped viruses, which infect hosts from phylogenetically distant archaeal lineages. Sulfolobus spindle-shaped virus 1 (SSV1) is the best known member of the family and was one of the first hyperthermophilic archaeal viruses to be isolated. SSV1 is an attractive model for understanding virus-host interactions in Archaea; however, the constituents and architecture of SSV1 particles remain only partially characterized. Here, we have conducted an extensive biochemical characterization of highly purified SSV1 virions and identified four virus-encoded structural proteins, VP1 to VP4, as well as one DNA-binding protein of cellular origin. The virion proteins VP1, VP3, and VP4 undergo posttranslational modification by glycosylation, seemingly at multiple sites. VP1 is also proteolytically processed. In addition to the viral DNA-binding protein VP2, we show that viral particles contain the Sulfolobus solfataricus chromatin protein Sso7d. Finally, we provide evidence indicating that SSV1 virions contain glycerol dibiphytanyl glycerol tetraether (GDGT) lipids, resolving a long-standing debate on the presence of lipids within SSV1 virions. A comparison of the contents of lipids isolated from the virus and its host cell suggests that GDGTs are acquired by the virus in a selective manner from the host cytoplasmic membrane, likely during progeny egress. Viruses infecting extremophilic archaea have evolved to withstand very high temperatures, low or high pH, or near-saturating salt concentrations (1-5). Remarkably, most of these viruses do not seem to be evolutionarily related to viruses of bacteria or eukaryotes and display a considerable diversity of unique virion morphotypes (3, 4). Indeed, 11 novel viral families have been established by the International Committee for the Taxonomy of Viruses (ICTV) for the classification of archaeal viruses, emphasizing the uniqueness of rod-shaped, spindle-shaped, dropletshaped, or even bottle-shaped particles that have never been observed among viruses infecting bacteria or eukaryotes (3). Functional studies proved to be highly challenging due to the lack of similarity between the protein sequences and structures of archaeal viruses and those from other viruses and cellular organisms (6-10). Among the morphotypes that are exclusively associated with archaea, spindle-shaped viruses are particularly widespread (11) and have been isolated from highly different environments, including deep-sea hydrothermal vents (12-14), hypersaline environments (15-18), anoxic freshwaters (19), cold Antarctic lakes (20), terrestrial hot springs (21-23), and acidic mines (24).Recently, we refined the evolutionary relationships among spindle-shaped viruses by assessing the morph...

“…Interestingly, the ATSV genome lacks most of the DNA-modifying proteins present in STSV1 and STSV2 (45). Several of the ATSV ORFs have homologs in other archaeal viruses, including 7 ORFs that make up a core set of genes carried by all or most large spindle virus genomes (ATSV, STSV1 and -2, ATV, and SMV1) (see Data Set S1 in the supplemental material) (48). These ORFs include the MCP (D135), a viral integrase (C242), 2 ATPases (F518 and D331), and 3 genes of unknown functions (F737, D1241, and B2246).…”

Section: Identification Of a Virus-like Contig From A Hot Spring Viramentioning

confidence: 99%

Acidianus Tailed Spindle Virus: a New Archaeal Large Tailed Spindle Virus Discovered by Culture-Independent Methods

Hochstein

Amenábar

Munson-McGee

et al. 2016

The field of viral metagenomics has expanded our understanding of viral diversity from all three domains of life (Archaea, Bacteria, and Eukarya). Traditionally, viral metagenomic studies provide information about viral gene content but rarely provide knowledge about virion morphology and/or cellular host identity. Here we describe a new virus, Acidianus tailed spindle virus (ATSV), initially identified by bioinformatic analysis of viral metagenomic data sets from a high-temperature (80°C) acidic (pH 2) hot spring located in Yellowstone National Park, followed by more detailed characterization using only environmental samples without dependency on culturing. Characterization included the identification of the large tailed spindle virion morphology, determination of the complete 70.8-kb circular double-stranded DNA (dsDNA) viral genome content, and identification of its cellular host. Annotation of the ATSV genome revealed a potential three-domain gene product containing an N-terminal leucine-rich repeat domain, followed by a likely posttranslation regulatory region consisting of high serine and threonine content, and a C-terminal ESCRT-III domain, suggesting interplay with the host ESCRT system. The host of ATSV, which is most closely related to Acidianus hospitalis, was determined by a combination of analysis of cellular clustered regularly interspaced short palindromic repeat (CRISPR)/Cas loci and dual viral and cellular fluorescence in situ hybridization (viral FISH) analysis of environmental samples and confirmed by culture-based infection studies. This work provides an expanded pathway for the discovery, isolation, and characterization of new viruses using culture-independent approaches and provides a platform for predicting and confirming virus hosts. IMPORTANCEVirus discovery and characterization have been traditionally accomplished by using culture-based methods. While a valuable approach, it is limited by the availability of culturable hosts. In this research, we report a virus-centered approach to virus discovery and characterization, linking viral metagenomic sequences to a virus particle, its sequenced genome, and its host directly in environmental samples, without using culture-dependent methods. This approach provides a pathway for the discovery, isolation, and characterization of new viruses. While this study used an acidic hot spring environment to characterize a new archaeal virus, Acidianus tailed spindle virus (ATSV), the approach can be generally applied to any environment to expand knowledge of virus diversity in all three domains of life. O ur knowledge and understanding of archaeal viruses (viruses that infect Archaea) are limited. Only 117 archaeal viruses are described at some level, with only a few being characterized in any significant depth (1-4). Remarkably, these relatively few archaeal viruses have formed 16 new virus families (5) and have expanded our appreciation of virion morphology, diversity, and gene content (5-7). Known archaeal viruses infect just 16 of 98 known gen...