Three-dimensional Reconstruction of the Surface Protein of the Extremely Thermophilic Archaebacterium Archaeoglobus fulgidus

Kessel, Martin; Volker, Susanne; Santarius, Ute; Huber, Robert; Baumeister, Wolfgang

doi:10.1016/s0723-2020(11)80187-6

Cited by 25 publications

(7 citation statements)

References 28 publications

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“…It is astonishing that the effect of glycosylation in archaea is not well characterized, despite the fact that most of the surface proteins, e.g. archaeal flagellins (Ng et al ., 2006), pilins (Ng et al ., 2011), S‐layer proteins (Mescher and Strominger, 1976; Kessel et al ., 1988; 1990; Sumper et al ., 1990; Zeitler et al ., 1998; Voisin et al ., 2005; Peyfoon et al ., 2010), and transport proteins (Albers et al ., 1999; Elferink et al ., 2001; Palmieri et al ., 2006) from diverse archaea being known to be modified by O ‐ and/or N ‐glycosylation.…”

Section: Discussionmentioning

confidence: 99%

Sulfoquinovose synthase – an important enzyme in the N‐glycosylation pathway of Sulfolobus acidocaldarius

Meyer

Zolghadr

Peyfoon

et al. 2011

Molecular Microbiology

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SummaryRecently, the Surface (S)-layer glycoprotein of the thermoacidophilic crenarchaeote Sulfolobus acidocaldarius was found to be N-glycosylated with a heterogeneous family of glycans, with the largest having a composition Glc1Man2GlcNAc2 plus 6-sulfoquinovose. However, genetic analyses of genes involved in the N-glycosylation process in Crenarchaeota were missing so far. In this study we identify a gene cluster involved in the biosynthesis of sulfoquinovose and important for the assembly of the S-layer N-glycans. A successful markerless in-frame deletion of agl3 resulted in a decreased molecular mass of the S-layer glycoprotein SlaA and the flagellin FlaB, indicating a change in the Nglycan composition. Analyses with nanoLC ES-MS/MS confirmed the presence of only a reduced trisaccharide structure composed of Man 1GlcNAc2, missing the sulfoquinovose, a mannose and glucose. Biochemical studies of the recombinant Agl3 confirmed the proposed function as a UDP-sulfoquinovose synthase. Furthermore, S. acidocaldarius cells lacking agl3 had a significantly lower growth rate at elevated salt concentrations compared with the background strain, underlining the importance of the N-glycosylation to maintain an intact and stable cell envelope, to enable the survival of S. acidocaldarius in its extreme environment.

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Section: Discussionmentioning

confidence: 99%

Sulfoquinovose synthase – an important enzyme in the N‐glycosylation pathway of Sulfolobus acidocaldarius

Meyer

Zolghadr

Peyfoon

et al. 2011

Molecular Microbiology

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“…However, if the formation of self-contained lattices were a principle of shape determination, why then are other archaea not shaped accordingly, especially as 2-D lattices from p1 to p6 symmetries have the capacity to form selfcontained cylinders (Paul et al, 1992)? The cells of Sulfolobales (Brock, 1981;Prüschenk et al, 1987), Desulfurococcales , Nanoarchaeum (Huber et al, 2002;Briegel, 2005), Archaeoglobus (Kessel et al, 1990) and of other archaea are rounded or irregularly shaped in thin-sectioned preparations. S-layers on a sphere, or on apparent half-spheres at the poles of rod-like cells, possess sites of dislocations (Harris and Scriven, 1970) and/or disclinations to cover the surface (Messner et al, 1986a;Pum et al, 1991).…”

Section: Assumption: S-layers Determine and Maintain The Cell Shapementioning

confidence: 99%

Are S-layers exoskeletons? The basic function of protein surface layers revisited

Engelhardt

2007

Journal of Structural Biology

137

121

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Surface protein or glycoprotein layers (Slayers) are common structures of the prokaryotic cell envelope. They are either associated with the peptidoglycan or outer membrane of bacteria, and constitute the only cell wall component of many archaea. Despite their occurrence in most of the phylogenetic branches of microorganisms, the functional significance of S-layers is assumed to be specific for genera or groups of organisms in the same environment rather than common to all prokaryotes. Functional aspects have usually been investigated with isolated S-layer sheets or proteins, which disregards the interactions between S-layers and the underlying cell envelope components. This study discusses the synergistic effects in cell envelope assemblies, the hypothetical role of S-layers for cell shape formation, and the existence of a common function in view of new insights.

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“…To reduce thickness of the sample and improve staining, cell ghost preparations were made from whole A. fulgidus cells as described in Section 2 and imaged after being negatively stained with a 1% UA solution ( Figure 1(c) ). The ordered S-layer coat surrounding the cell membrane is apparent [ 11 ], whereas the granules usually present within either were absent or did not appear as uniformly dark electron dense bodies. This result may be due to loss of structural integrity during ghost preparation process, whereby most of the cellular cytoplasm is extracted leaving behind the cell membrane with attached S-layer proteins.…”

Section: Resultsmentioning

confidence: 99%

“…Embedding whole cells in vitreous ice preserves their structures in a natural state and eliminates the artifacts associated with staining ( Figure 2(a) ). These cryoET reconstructions of A. fulgidus cells reveal typical S-layer envelope surrounding the cellular monolayer membrane composed of C40 isoprenoid diether lipids [ 11 , 12 ]. The reconstructions also show that the A. fulgidus cells are coccoid to irregular in shape and approximately 1 μ m in diameter.…”

Section: Resultsmentioning

confidence: 99%

Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting inArchaeoglobus fulgidusCells

Toso

Javed

Czornyj

et al. 2016

Archaea

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Inorganic storage granules have long been recognized in bacterial and eukaryotic cells but were only recently identified in archaeal cells. Here, we report the cellular organization and chemical compositions of storage granules in the Euryarchaeon, Archaeoglobus fulgidus strain VC16, a hyperthermophilic, anaerobic, and sulfate-reducing microorganism. Dense granules were apparent in A. fulgidus cells imaged by cryo electron microscopy (cryoEM) but not so by negative stain electron microscopy. Cryo electron tomography (cryoET) revealed that each cell contains one to several dense granules located near the cell membrane. Energy dispersive X-ray (EDX) spectroscopy and scanning transmission electron microscopy (STEM) show that, surprisingly, each cell contains not just one but often two types of granules with different elemental compositions. One type, named iron sulfide body (ISB), is composed mainly of the elements iron and sulfur plus copper; and the other one, called polyphosphate body (PPB), is composed of phosphorus and oxygen plus magnesium, calcium, and aluminum. PPBs are likely used for energy storage and/or metal sequestration/detoxification. ISBs could result from the reduction of sulfate to sulfide via anaerobic energy harvesting pathways and may be associated with energy and/or metal storage or detoxification. The exceptional ability of these archaeal cells to sequester different elements may have novel bioengineering applications.

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Three-dimensional Reconstruction of the Surface Protein of the Extremely Thermophilic Archaebacterium Archaeoglobus fulgidus

Cited by 25 publications

References 28 publications

Sulfoquinovose synthase – an important enzyme in the N‐glycosylation pathway of Sulfolobus acidocaldarius

Sulfoquinovose synthase – an important enzyme in the N‐glycosylation pathway of Sulfolobus acidocaldarius

Are S-layers exoskeletons? The basic function of protein surface layers revisited

Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting inArchaeoglobus fulgidusCells

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