Eukaryotic-Like Virus Budding in
            <i>Archaea</i>

Quemin, Emmanuelle R. J.; Chlanda, Petr; Sachse, Martin; Forterre, Patrick; Prangishvili, David; Krupovìč, Mart

doi:10.1128/mbio.01439-16

Cited by 62 publications

(64 citation statements)

References 19 publications

(28 reference statements)

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“…Buds were generated when the cells of the wild type strain were infected with STSV2, a membrane‐enveloped virus (Fig. ), and our finding was consistent with a recent report of budding of archaeal fusiform virus SSV1 (Quemin et al ., ). Budding was also observed in cells over‐expressing ESCRT‐III‐3 but not ESCRT‐III, ESCRT‐III‐1 and −2 (Fig.…”

Section: Discussionmentioning

confidence: 98%

Functional assignment of multiple ESCRT‐III homologs in cell division and budding in Sulfolobus islandicus

Liu

Gao

et al. 2017

Molecular Microbiology

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The archaea Sulfolobus utilizes the ESCRT-III-based machinery for cell division. This machinery comprises three proteins: CdvA, Eukaryotic-like ESCRT-III and Vps4. In addition to ESCRT-III, Sulfolobus cells also encode three other ESCRT-III homologs termed ESCRT-III-1, -2 and -3. Herein, we show that ESCRT-III-1 and -2 in S. islandicus REY15A are localized at midcell between segregating chromosomes, indicating that both are involved in cell division. Genetic analysis reveals that escrt-III-2 is indispensable for cell viability and cells with reduced overall level of ESCRT-III-1 exhibit growth retardation and cytokinesis defect with chain-like cell morphology. In contrast, escrt-III-3 is dispensable for cell division. We show that S. islandicus REY15A cells generate buds when infected with S. tengchongensis spindle shaped-virus 2 (STSV2) or when ESCRT-III-3 is over-expressed. Interestingly, Δescrt-III-3 cells infected with STSV2 do not produce buds. These results suggest that ESCRT-III-3 plays an important role in budding. In addition, cells over-expressing the C-terminal truncated mutants of ESCRT-III, ESCRT-III-1 and ESCRT-III-2 are maintained predominantly at the early, late, and membrane abscission stages of cell division respectively, suggesting a crucial role of the ESCRTs at different stages of membrane ingression. Intriguingly, intercellular bridge and midbody-like structures are observed in cells over-expressing MIM2-truncated mutant of ESCRT-III-2.

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Section: Discussionmentioning

confidence: 98%

Functional assignment of multiple ESCRT‐III homologs in cell division and budding in Sulfolobus islandicus

Liu

Gao

et al. 2017

Molecular Microbiology

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“…Compensating for the absence of S-layer by forming a strong barrier at the site of cell division is hypothesized to be one role for Cdv proteins (27). The S-layer is believed to be a receptor for viruses and has been shown to change structure after viral induction and provide a barrier to virus egress during maturation of the SSV viral particle (28). No generalized function for the S-layer in Archaea has been defined as no archaeal S-layer deficient mutants have been characterized.…”

Section: Introductionmentioning

confidence: 99%

Revealing S-layer Functions in the Hyperthermophilic Crenarchaeon Sulfolobus islandicus

Zhang

et al. 2018

Preprint

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36The crystalline surface layer (S-layer), consisting of two glycoproteins SlaA and SlaB, is 37 considered to be the exclusive component of the cell envelope outside of the cytoplasmic 38 membrane in Sulfolobus species. Although biochemically and structurally characterized, the S-39 layer in vivo functions remain largely elusive in Archaea. Here, we investigate how the S-layer 40 genes contribute to the S-layer architecture and affect cellular physiology in a crenarchaeal 41 model, Sulfolobus islandicus M.16.4. Electron micrographs of mutant cells lacking slaA or both 42 slaA and slaB confirm the absence of the outermost layer (SlaA), whereas cells with intact, 43 partially, or completely detached SlaA are observed for the ΔslaB mutant. Importantly, we 44 identify a novel S-layer-associated protein M164_1049, which does not functionally replace its 45 homolog SlaB but likely assists SlaB to stabilize SlaA. Additionally, we find that mutants 46 deficient in SlaA form large cell aggregates and the individual cell size varies significantly. The 47 slaB gene deletion also causes noticeable cellular aggregation, but the size of those aggregates 48 is smaller when compared to ΔslaA and ΔslaAB mutants. We further show the ΔslaA mutant 49 cells exhibit more sensitivity to hyperosmotic stress but are not reduced to wild-type cell size. 50Finally, we demonstrate that the ΔslaA mutant contains aberrant chromosome copy numbers 51 not seen in wild-type cells where the cell cycle is tightly regulated. Together these data suggest 52 that the lack of slaA results in either cell fusion or irregularities in cell division. Our studies 53 provide novel insights into the physiological and cellular functions of the S-layer in Archaea. 55Significance 56Rediscovery of the ancient evolutionary relationship between archaea and eukaryotes has 57 revitalized interest in archaeal cell biology. Key to understanding the archaeal cell is the S-58 layer which is ubiquitous in Archaea but whose in vivo function is unknown. In this study, we 59 genetically dissect how the two well-known S-layer genes as well as a newly identified S-layer-60 associated-protein-encoding gene contribute to the S-layer architecture in a hyperthermophilic 61 crenarchaeal model S. islandicus. We provide genetic evidence for the first time showing that 62 the slaA gene is a key cell morphology determinant and may play a role in Sulfolobus cell 63 division or cell fusion.64 65 66 67 68 69 70 71 72The primary interface between the cell and its environment is a multi-functional cellular 73 envelope. Comprised in this structure in some bacterial and most archaeal cells is a 74 proteinaceous 2D-crystalline matrix coating the outside of the cell called the surface layer (S-75 layer). Despite its broad distribution in cells from two domains, a generalized function of the 76 S-layer has not been identified. One unifying concept suggests the S-layer functions as an 77 exoskeleton that interacts with other proteins in the cell membrane to coordinate diverse 78 internal and externa...

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“…There are reasons to believe that the known variety of archaeal viruses represents no more than the tip of an iceberg and that comprehensive information on them may shed light on the problems of origin and evolution of viruses and virus-host interactions (16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28).…”

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confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

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Encapsidation of genetic material into polyhedral particles is one of the most common structural solutions employed by viruses infecting hosts in all three domains of life. Here, we describe a new virus of hyperthermophilic archaea, Sulfolobus polyhedral virus 1 (SPV1), which condenses its circular double-stranded DNA genome in a manner not previously observed for other known viruses. The genome complexed with virion proteins is wound up sinusoidally into a spherical coil which is surrounded by an envelope and further encased by an outer polyhedral capsid apparently composed of the 20-kDa virion protein. Lipids selectively acquired from the pool of host lipids are integral constituents of the virion. None of the major virion proteins of SPV1 show similarity to structural proteins of known viruses. However, minor structural proteins, which are predicted to mediate host recognition, are shared with other hyperthermophilic archaeal viruses infecting members of the order Sulfolobales. The SPV1 genome consists of 20,222 bp and contains 45 open reading frames, only one-fifth of which could be functionally annotated.IMPORTANCE Viruses infecting hyperthermophilic archaea display a remarkable morphological diversity, often presenting architectural solutions not employed by known viruses of bacteria and eukaryotes. Here we present the isolation and characterization of Sulfolobus polyhedral virus 1, which condenses its genome into a unique spherical coil. Due to the original genomic and architectural features of SPV1, the virus should be considered a representative of a new viral family, "Portogloboviridae."KEYWORDS archaea, hyperthermophile, viral genome, virion structure O ne of the most unexpected results of recent studies on viral diversity is the unveiling of astounding morphological variety of DNA viruses in geothermal environments with temperatures exceeding 80°C (1). Hardly over two dozen viruses isolated from such environments, all parasitizing hyperthermophilic members of the domain Archaea, display diverse virion shapes, many of which have not been observed among viruses from the two other domains of life, Bacteria and Eukarya. Due to distinct genome compositions and peculiar morphological properties of these viruses, 11 new virus families were established by the International Committee on Taxonomy of Viruses (ICTV) for the classification of these viruses (1-4).The remarkable morphological diversity of hyperthermophilic archaeal viruses radically contrasts the limited structural diversity of double-stranded DNA (dsDNA) viruses of Bacteria, nearly all of which, with the exception of several pleomorphic species, have icosahedral particles, with or without helical tails (5). The existing picture seems to accurately reflect the actual differences between bacterial and archaeal viruses. The morphological landscape of bacterial viruses is formed by more than six thousand species, whereas that of hyperthermophilic archaeal viruses is formed by only a couple of dozen known species. Moreover, while no new morpho...

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Eukaryotic-Like Virus Budding in Archaea

Cited by 62 publications

References 19 publications

Functional assignment of multiple ESCRT‐III homologs in cell division and budding in Sulfolobus islandicus

Functional assignment of multiple ESCRT‐III homologs in cell division and budding in Sulfolobus islandicus

Revealing S-layer Functions in the Hyperthermophilic Crenarchaeon Sulfolobus islandicus

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

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