Molecular tiling on the surface of a bacterial spore – the exosporium of the <i>Bacillus anthracis/cereus/thuringiensis</i> group

Terry, Cassandra; Jiang, Shuo; Radford, David; Wan, Qiang; Tzokov, Svetomir B.; Moir, Anne; Bullough, Per A.

doi:10.1111/mmi.13650

Cited by 37 publications

(69 citation statements)

References 50 publications

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“…Similar to UDP-GlcNAc 2-epimerase, the genome of B. anthracis also includes two genes, galE1 and galE2, for UDP-Glc 4-epimerase, an enzyme that catalyzes the reversible interconversion of UDP-Glc and UDP-Gal (19). One of these two genes, galE2, is expressed only during B. anthracis sporulation, providing UDP-Gal and UDP-GalNAc substrates for the glycosylation of BclA, an exosporium protein in the outer spore nap that is produced by all members of the B. cereus sensu lato group (21,(43)(44)(45). In contrast, galE1 is only expressed during vegetative growth and provides UDP-Gal for the galactosylation of the SCWP in B. anthracis.…”

Section: Discussionmentioning

confidence: 99%

Galactosylation of the Secondary Cell Wall Polysaccharide of Bacillus anthracis and Its Contribution to Anthrax Pathogenesis

Château

Lunderberg

et al. 2018

J Bacteriol

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, the causative agent of anthrax disease, elaborates a secondary cell wall polysaccharide (SCWP) that is essential for bacterial growth and cell division. SCWP is comprised of trisaccharide repeats with the structure, [→4)-β-ManNAc-(1→4)-β-GlcNAc(3-α-Gal)-(1→6)-α-GlcNAc(3-α-Gal, 4-β-Gal)-(1→] The genes whose products promote the galactosylation of SCWP are not yet known. We show here that the expression of, encoding a UDP-glucose 4-epimerase necessary for the synthesis of UDP-galactose, is required for SCWP galactosylation. The mutant assembles surface (S) layer and S layer-associated proteins that associate with ketal-pyruvylated SCWP via their S layer homology domains similarly to wild-type , but the mutant displays a defect in γ-phage murein hydrolase binding to SCWP. Furthermore, deletion of diminishes the capsulation of with poly-d-γ-glutamic acid (PDGA) and causes a reduction in bacterial virulence. These data suggest that SCWP galactosylation is required for the physiologic assembly of the cell wall envelope and for the pathogenesis of anthrax disease. Unlike virulent isolates, strain CDC684 synthesizes secondary cell wall polysaccharide (SCWP) trisaccharide repeats without galactosyl modification, exhibits diminished growth in broth cultures, and is severely attenuated in an animal model of anthrax. To examine whether SCWP galactosylation is a requirement for anthrax disease, we generated variants of strains Sterne 34F2 and Ames lacking UDP-glucose 4-epimerase by mutating the genes and We identified as necessary for SCWP galactosylation. Deletion of decreased the poly-d-γ-glutamic acid (PDGA) capsulation of the vegetative form of and increased the bacterial inoculum required to produce lethal disease in mice, indicating that SCWP galactosylation is indeed a determinant of anthrax disease.

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Section: Discussionmentioning

confidence: 99%

Galactosylation of the Secondary Cell Wall Polysaccharide of Bacillus anthracis and Its Contribution to Anthrax Pathogenesis

Château

Lunderberg

et al. 2018

J Bacteriol

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“…Terry et al . () propose that ExsY forms the repeating unit comprising most of the crystalline lattice of the exosporium basal layer. The recombinant CotY protein was also found to be capable of self‐assembly, but less efficiently compared to ExsY.…”

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confidence: 99%

“…Electron crystallography studies of these arrays indicated that they exhibit the open lattice of hexameric ring-like structures that was extraordinarily similar to that observed in the native exosporia of the B. cereus family spores. Terry et al (2017) propose that ExsY forms the repeating unit comprising most of the crystalline lattice of the exosporium basal layer. The recombinant CotY protein was also found to be capable of self-assembly, but less efficiently compared to ExsY.…”

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confidence: 99%

Assembly of the outermost spore layer: pieces of the puzzle are coming together

Stewart

2017

Molecular Microbiology

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Summary Certain endospore-forming soil dwelling bacteria are important human, animal, or insect pathogens. These organisms produce spores containing an outer layer, the exosporium. The exosporium is the site of interactions between the spore and the soil environment and between the spore and the infected host during the initial stages of infection. The composition and assembly process of the exosporium are poorly understood. This is partly due to the extreme stability of the exosporium that has proven to be refractive to existing methods to deconstruct the intact structure into its component parts. Although more than 20 proteins have been identified as exosporium-associated, their abundance, relationship to other proteins, and the processes by which they are assembled to create the exosporium are largely unknown. In this issue of Molecular Microbiology, Terry, Jiang, and colleagues in Per Bullough’s laboratory show that the ExsY protein is a major structural protein of the exosporium basal layer of B. cereus family spores and that it can self-assemble into complex structures that possess many of the structural features characteristic of the exosporium basal layer. The authors refined a model for exosporium assembly. Their findings may have implications for exosporium formation in other spore forming bacteria, including Clostridium species.

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“…Orthologues of CotW and CotX are also encoded in the genomes of several B. cereus strains but are absent from B. anthracis (27), indicating that they do not function as structural components of exosporia across the genus. Similarly, the B. subtilis CotY crust protein and its paralogue ExsY, both of which are absent from the B. megaterium genome, appear to have crucial structural roles in the exosporia of B. cereus and B. anthracis (9,30,31).…”

Section: Discussionmentioning

confidence: 99%

“…The exosporium in B. cereus family spores is a thin, sheath-like structure that is typically significantly larger and more flexible than the densely packed spore within. Its biological function(s) has not been unequivocally defined; however, a series of electron crystallographic studies have revealed that it has an ordered structure punctuated with an array of what appear to be openings (7)(8)(9)(10). These openings support the often-stated idea that the exosporium, as the spore's interface with the environment, serves in one capacity as a molecular sieve (8).…”

mentioning

confidence: 95%

Orthologues of Bacillus subtilis Spore Crust Proteins Have a Structural Role in the Bacillus megaterium QM B1551 Spore Exosporium

Manetsberger

Ghosh

Hall

et al. 2018

Appl Environ Microbiol

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The exosporium ofBacillus megateriumQM B1551 spores is morphologically distinct from exosporia observed for the spores of many other species. Previous work has demonstrated that unidentified genes carried on one of the large indigenous plasmids are required for the assembly of theBacillus megateriumexosporium. Here, we provide evidence that pBM600-encoded orthologues of theBacillus subtilisCotW and CotX proteins, which form the crust layer in spores of that species, are structural components of theBacillus megateriumQM B1551 spore exosporium. The introduction of plasmid-bornecotWand orthologouscotXgenes to the PV361 strain, which lacks all indigenous plasmids and produces spores that are devoid of an exosporium, results in the development of spores with a rudimentary exosporium-type structure. Additionally, purified recombinant CotW protein is shown to assemble at the air-water interface to form thin sheets of material, which is consistent with the idea that this protein may form a basal layer in theBacillus megateriumQM B1551 exosporium.IMPORTANCEWhen starved of nutrients, some bacterial species develop metabolically dormant spores that can persist in a viable state in the environment for several years. The outermost layers of spores are of particular interest since (i) these represent the primary site for interaction with the environment and (ii) the protein constituents may have biotechnological applications. The outermost layer, or exosporium, inBacillus megateriumQM B1551 spores is of interest, as it is morphologically distinct from the exosporia of spores of the pathogenicBacillus cereusfamily. In this work, we provide evidence that structurally important protein constituents of theBacillus megateriumexosporium are different from those in theBacillus cereusfamily. We also show that one of these proteins, when purified, can assemble to form sheets of exosporium-like material. This is significant, as it indicates that spore-forming bacteria employ different proteins and mechanisms of assembly to construct their external layers.

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Molecular tiling on the surface of a bacterial spore – the exosporium of the Bacillus anthracis/cereus/thuringiensis group

Cited by 37 publications

References 50 publications

Galactosylation of the Secondary Cell Wall Polysaccharide of Bacillus anthracis and Its Contribution to Anthrax Pathogenesis

Galactosylation of the Secondary Cell Wall Polysaccharide of Bacillus anthracis and Its Contribution to Anthrax Pathogenesis

Assembly of the outermost spore layer: pieces of the puzzle are coming together

Orthologues of Bacillus subtilis Spore Crust Proteins Have a Structural Role in the Bacillus megaterium QM B1551 Spore Exosporium

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