Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components

Ellen, Albert F.; Albers, Sonja‐Verena; Huibers, Wim; Pitcher, Angela; Hobel, Cédric F.V.; Schwarz, Heinz; Folea, Mihaela; Schouten, Stefan; Boekema, Egbert J.; Poolman, Bert; Driessen, Arnold J. M.

doi:10.1007/s00792-008-0199-x

Cited by 150 publications

(179 citation statements)

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“…Notably, the ratio of different lipid species in the virions was different from that found in the cytoplasmic membrane of the host cells, suggesting a selective incorporation of lipids into the virion. Similarly, lipid composition of Sulfolobus turreted icosahedral virus, which has an internal membrane, and lipid content of membrane vesicles produced by S. solfataricus were found to differ considerably from that of the cellular membrane (68,85). Interestingly, the hyperhalophilic spindle-shaped virus His1 does not appear to contain free lipids; instead, its major capsid protein, homologous to VP1/VP3 of SSV1, was concluded to be covalently modified by a lipid moiety (48), suggesting that distinct spindleshaped viruses use different mechanisms for lipid acquisition from the host.…”

Section: Discussionmentioning

confidence: 98%

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

Quemin

Pietilä

Oksanen

et al. 2015

J Virol

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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...

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Section: Discussionmentioning

confidence: 98%

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

Quemin

Pietilä

Oksanen

et al. 2015

J Virol

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“…In addition, archaea also produce and secrete vesicles with defined cargoes. Proteins homologous to components of the endosomal sorting complex required for transport have been found in vesicles secreted by Sulfolobus species (48). Based on those observations, it is tempting to speculate that OMV formation with defined protein cargo in prokaryotes may be an ancient process related to vesicle formation in eukaryotes.…”

Section: Discussionmentioning

confidence: 99%

Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles

Haurat¹,

Aduse‐Opoku

Rangarajan

et al. 2011

Journal of Biological Chemistry

269

290

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In contrast to the well established multiple cellular roles of membrane vesicles in eukaryotic cell biology, outer membrane vesicles (OMV) produced via blebbing of prokaryotic membranes have frequently been regarded as cell debris or microscopy artifacts. Increasingly, however, bacterial membrane vesicles are thought to play a role in microbial virulence, although it remains to be determined whether OMV result from a directed process or from passive disintegration of the outer membrane. Here we establish that the human oral pathogen Porphyromonas gingivalis has a mechanism to selectively sort proteins into OMV, resulting in the preferential packaging of virulence factors into OMV and the exclusion of abundant outer membrane proteins from the protein cargo. Furthermore, we show a critical role for lipopolysaccharide in directing this sorting mechanism. The existence of a process to package specific virulence factors into OMV may significantly alter our current understanding of host-pathogen interactions.

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“…Membrane vesicles and the culture supernatant fraction were obtained as described previously (7). Stationary grown cultures of 800 ml were cooled down on ice for 20 min, followed by a low spin centrifugation (10 min, 12,000 ϫ g, 4°C) to remove intact cells.…”

Section: Methodsmentioning

confidence: 99%

The Sulfolobicin Genes of Sulfolobus acidocaldariusEncode Novel Antimicrobial Proteins

et al. 2011

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Crenarchaea, such as Sulfolobus acidocaldarius and Sulfolobus tokodaii, produce antimicrobial proteins called sulfolobicins. These antimicrobial proteins inhibit the growth of closely related species. Here we report the identification of the sulfolobicin-encoding genes in S. acidocaldarius. The active sulfolobicin comprises two proteins that are equipped with a classical signal sequence. These proteins are secreted by the cells and found to be membrane vesicle associated. Gene inactivation studies demonstrate that both proteins are required for the bacteriostatic antimicrobial activity. Sulfolobicins constitute a novel class of antimicrobial proteins without detectable homology to any other protein.

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Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components

Cited by 150 publications

References 50 publications

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

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

Selective Sorting of Cargo Proteins into Bacterial Membrane Vesicles

The Sulfolobicin Genes of Sulfolobus acidocaldariusEncode Novel Antimicrobial Proteins

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