S-layer

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An S-layer (surface layer) is a part of the cell envelope commonly found in bacteria, as well as among archaea .[1] It consists of a monomolecular layer composed of identical proteins or glycoproteins. This two-dimensional structure is built via self-assembly and encloses the whole cell surface. Thus, the S-layer protein can represent up to 10–15% of the whole protein content of a cell. [2] [3] [4] S-layer proteins are poorly conserved or not conserved at all, and can differ markedly even between related species. Depending on species, the S-layers have a thickness between 5 and 25 nm and possess identical pores with 2–8 nm in diameter.[5] S-layers exhibit either an oblique (p1, p2), square (p4) or hexagonal (p3, p6) lattice symmetry. Depending on the lattice symmetry, the S-layer is composed of one (P1), two (P2), three (P3), four (P4), or six (P6) identical protein subunits, respectively. The center-to-center spacings (or unit cell dimensions) between these subunits range between 2.5 and 35 nm.

Fixation of S-layers in the cell wall

  • In Gram-negative bacteria, S-layers are associated to the lipopolysaccharides via ionic, carbohydrate–carbohydrate, protein–carbohydrate interactions and/or protein–protein interactions.
  • In Gram-positive bacteria whose S-layers often contain surface layer homology (SLH) domains, the binding occurs to the peptidoglycan and to a secondary cell wall polymer (e.g., teichoic acids). In the absence of SLH domains, the binding occurs via electrostatic interactions between the positively charged N-terminus of the S-layer protein and a negatively charged secondary cell wall polymer.
  • In Gram-negative archaea, S-layer proteins possess a hydrophobic anchor that is associated with the underlying lipid membrane.
  • In Gram-positive archaea, the S-layer proteins bind to pseudomurein or to methanochondroitin.

Biological functions of the S-layer

For many bacteria, the S-layer represents the outermost interaction zone with their respective environment. Its functions are very diverse and vary from species to species. In Archaea the S-layer is the only cell wall component and, therefore, is important for mechanical stabilization. Additional functions associated with S-layers include:

  • protection against bacteriophages, Bdellovibrios, and phagocytosis
  • resistance against low pH
  • barrier against high-molecular-weight substances (e.g., lytic enzymes)
  • adhesion (for glycosylated S-layers)
  • stabilisation of the membrane
  • provision of adhesion sites for exoproteins
  • provision of a periplasmic compartment in Gram-positive prokaryotes together with the peptidoglycan and the cytoplasmic membranes

S-layer structure

While ubiquitous among Archaea, and common in bacteria, the S-layers of diverse organisms have unique structural properties, including symmetry and unit cell dimensions, due to fundamental differences in their constituent building blocks. Sequence analyses of S-layer proteins have predicted that S-layer proteins have sizes of 40-200 kDa and may be composed of multiple domains some of which may be structurally related. Since their discovery in the 1950s[6] S-layer structure has been investigated extensively by electron microscopy and medium resolution images of S-layers from these analyses has provided useful information on overall S-layer morphology. High-resolution structures of an archaeal S-layer protein (MA0829 from Methanosarcina acetivorans C2A) of the Methanosarcinales S-layer Tile Protein family and a bacterial S-layer protein (SbsB), from Geobacillus stearothermophilus PV72, have recently been determined by X-ray crystallography.[7][8] In contrast with existing crystal structures, which have represented individual domains of S-layer proteins or minor proteinaceous components of the S-layer, the MA0829 and SbsB structures have allowed high resolution models of the M. acetivorans and G. stearothermophilus S-layers to be proposed. These models exhibit hexagonal (p6) and oblique (p2) symmetry, for M. acetivorans and G. stearothermophilus S-layers, respectively, and their molecular features, including dimensions and porosity, are in good agreement with data from electron microscopy studies of archaeal and bacterial S-layers.

References

  1. S-layers on cell walls of cyanobacteria Micron Volume 33, Issue 3, January 2002, Pages 257–277; doi:10.1016/S0968-4328(01)00031-2
  2. Messner P, Sleytr U (1992). "Crystalline bacterial cell-surface layers". Adv. Microb. Physiol. 33: 213–75. doi:10.1016/S0065-2911(08)60218-0. PMID 1636510. 
  3. Pum D, Messner P, Sleytr U (1991). "Role of the S layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense". J. Bacteriol. 173 (21): 6865–73. PMC 209039. PMID 1938891. 
  4. Sleytr U, Messner P, Pum D, Sára M (1993). "Crystalline bacterial cell surface layers". Mol. Microbiol. 10 (5): 911–6. doi:10.1111/j.1365-2958.1993.tb00962.x. PMID 7934867. 
  5. Sleytr U, Bayley H, Sára M, Breitwieser A, Küpcü S, Mader C, Weigert S, Unger F, Messner P, Jahn-Schmid B, Schuster B, Pum D, Douglas K, Clark N, Moore J, Winningham T, Levy S, Frithsen I, Pankovc J, Beale P, Gillis H, Choutov D, Martin K (1997). "Applications of S-layers". FEMS Microbiol. Rev. 20 (1–2): 151–75. doi:10.1016/S0168-6445(97)00044-2. PMID 9276930. 
  6. Houwink, AL (1953). "A macromolecular mono-layer in the cell wall of Spirillum spec.". Biochim Biophys Acta. 10 (3): 360–6. PMID 13058992. 
  7. Arbing MA, Chan S, Shin A, Phan T, Ahn CJ, Rohlin L, Gunsalus RP (2012). "Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans.". Proc Natl Acad Sci U S A. 109 (29): 11812–7. doi:10.1073/pnas.1120595109. PMC 3406845. PMID 22753492. 
  8. Baranova E, Fronzes R, Garcia-Pino A, Van Gerven N, Papapostolou D, Péhau-Arnaudet G, Pardon E, Steyaert J, Howorka S, Remaut H (2012). "SbsB structure and lattice reconstruction unveil Ca2+ triggered S-layer assembly". Nature 487 (7405): 119–22. doi:10.1038/nature11155. PMID 22722836. 
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