S-layer

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An S-layer (surface layer) is a part of the cell envelope found in almost all archaea, as well as in many types of bacteria. [1] [2] The S-layers of both archaea and bacteria consists of a monomolecular layer composed of only one (or, in a few cases, two) identical proteins or glycoproteins. [3] This structure is built via self-assembly and encloses the whole cell surface. Thus, the S-layer protein can represent up to 15% of the whole protein content of a cell. [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 2–8 nm in diameter. [5]

Contents

The terminology “S-layer” was used the first time in 1976. [6] The general use was accepted at the "First International Workshop on Crystalline Bacterial Cell Surface Layers, Vienna (Austria)" in 1984, and in the year 1987 S-layers were defined at the European Molecular Biology Organization Workshop on “Crystalline Bacterial Cell Surface Layers”, Vienna as “Two-dimensional arrays of proteinaceous subunits forming surface layers on prokaryotic cells” (see "Preface", page VI in Sleytr "et al. 1988" [7] ). For a brief summary on the history of S-layer research see "References". [2] [8]

Location of S-layers

Schematic illustration of the supramolecular architecture of the major classes of prokaryotic cell envelopes containing surface (S) layers. S-layers in archaea with glycoprotein lattices as exclusive wall component are composed either of mushroom-like subunits with pillar-like, hydrophobic trans-membrane domains (a), or lipid-modified glycoprotein subunits (b). Individual S-layers can be composed of glycoproteins possessing both types of membrane anchoring mechanisms. Few archaea possess a rigid wall layer (e.g. pseudomurein in methanogenic organisms) as intermediate layer between the plasma membrane and the S-layer (c). In Gram-positive bacteria (d) the S-layer (glyco)proteins are bound to the rigid peptidoglycan-containing layer via secondary cell wall polymers. In Gram-negative bacteria (e) the S-layer is closely associated with the lipopolysaccharide of the outer membrane. Figure and figure legend were copied from Sleytr et al. 2014, which is available under a Creative Commons Attribution 3.0 International (CC BY 3.0) licence . CW-Architecture 1.png
Schematic illustration of the supramolecular architecture of the major classes of prokaryotic cell envelopes containing surface (S) layers. S-layers in archaea with glycoprotein lattices as exclusive wall component are composed either of mushroom-like subunits with pillar-like, hydrophobic trans-membrane domains (a), or lipid-modified glycoprotein subunits (b). Individual S-layers can be composed of glycoproteins possessing both types of membrane anchoring mechanisms. Few archaea possess a rigid wall layer (e.g. pseudomurein in methanogenic organisms) as intermediate layer between the plasma membrane and the S-layer (c). In Gram-positive bacteria (d) the S-layer (glyco)proteins are bound to the rigid peptidoglycan-containing layer via secondary cell wall polymers. In Gram-negative bacteria (e) the S-layer is closely associated with the lipopolysaccharide of the outer membrane. Figure and figure legend were copied from Sleytr et al. 2014, which is available under a Creative Commons Attribution 3.0 International (CC BY 3.0) licence CC-BY icon.svg .

Biological functions of the S-layer

For many bacteria, the S-layer represents the outermost interaction zone with their respective environment. [9] [2] Its functions are very diverse and vary from species to species. In many archaeal species the S-layer is the only cell wall component and, therefore, is important for mechanical and osmotic stabilization. The S-layer is considered to be porous, which contributes to many of its functions. [10] Additional functions associated with S-layers include:

A great example of a bacterium which utilizes the biological functions of the S-layer is Clostridioides difficile. In C. difficile, the S-layer has helped with biofilm formation, host cell adhesion, and immunomodulation through cell signaling of the host response. [18]

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. [19] 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 the first evidence of a macromolecular array on a bacterial cell wall fragment in the 1950s [20] 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. [21] [22] 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. [6]

In general, S-layers exhibit either oblique (p1, p2), square (p4) or hexagonal (p3, p6) lattice symmetry. Depending on the lattice symmetry, each morphological unit of the S-layer is composed of one (p1), two (p2), three (p3), four (p4), or six (p6) identical protein subunits. The center-to-center spacing (or unit cell dimensions) between these subunits range from 4 to 35 nm. [2]

Self-assembly

In vivo assembly

Assembly of a highly ordered coherent monomolecular S-layer array on a growing cell surface requires a continuous synthesis of a surplus of S-layer proteins and their translocation to sites of lattice growth. [23] Moreover, information concerning this dynamic process were obtained from reconstitution experiments with isolated S-layer subunits on cell surfaces from which they had been removed (homologous reattachment) or on those of other organisms (heterologous reattachment). [24]

In vitro assembly

S-layer proteins have the natural capability to self-assemble into regular monomolecular arrays in solution and at interfaces, such as solid supports, the air-water interface, lipid films, liposomes, emulsomes, nanocapsules, nanoparticles or micro beads. [2] [25] S-layer crystal growth follows a non-classical pathway in which a final refolding step of the S-layer protein is part of the lattice formation. [26] [27]

Application

Native S-layer proteins have already been used three decades ago in the development of biosensors and ultrafiltration membranes. Subsequently, S-layer fusion proteins with specific functional domains (e.g. enzymes, ligands, mimotopes, antibodies or antigens) allowed to investigate completely new strategies for functionalizing surfaces in the life sciences, such as in the development of novel affinity matrices, mucosal vaccines, biocompatible surfaces, micro carriers and encapsulation systems, or in the material sciences as templates for biomineralization. [2] [28] [29] [30]

Related Research Articles

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<span class="mw-page-title-main">Archaea</span> Domain of single-celled organisms

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<span class="mw-page-title-main">Uwe B. Sleytr</span> Austrian biologist

Uwe B. Sleytr is an emeritus professor of microbiology and the former head of the Department of Nanobiotechnology at the University of Natural Resources and Life Sciences, Vienna. He is a full member of the Division of Mathematics and Natural Sciences of the Austrian Academy of Sciences and has published approximately 420 scientific papers, 5 books and several patents.

References

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  11. 1 2 Farci D, Slavov C, Tramontano E, Piano D (2016). "The S-layer Protein DR_2577 Binds Deinoxanthin and under Desiccation Conditions Protects against UV-Radiation in Deinococcus radiodurans". Frontiers in Microbiology. 7: 155. doi: 10.3389/fmicb.2016.00155 . PMC   4754619 . PMID   26909071.
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  13. ↑ Rothbauer M, Küpcü S, Sticker D, Sleytr UB, Ertl P (2013). "Exploitation of S-layer Anisotropy: pH-dependent Nanolayer Orientation for Cellular Micropatterning". ACS Nano. 7 (9): 8020–8030. doi:10.1021/nn403198a. PMID   24004386.
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  17. ↑ Sára M, Sleytr, UB (1987). "Production and characteristics of ultrafiltration membranes with uniform pores from two-dimensional arrays of proteins". J. Membr. Sci. 33 (1): 27–49. doi:10.1016/S0376-7388(00)80050-2.
  18. ↑ Ormsby, Michael J.; Vaz, Filipa; Kirk, Joseph A.; Barwinska-Sendra, Anna; Hallam, Jennifer C.; Lanzoni-Mangutchi, Paola; Cole, John; Chaudhuri, Roy R.; Salgado, Paula S.; Fagan, Robert P.; Douce, Gillian R. (2023-06-29). "An intact S-layer is advantageous to Clostridioides difficile within the host". PLOS Pathogens. 19 (6): e1011015. doi: 10.1371/journal.ppat.1011015 . ISSN   1553-7374. PMC   10310040 . PMID   37384772.
  19. ↑ Pavkov-Keller T, Howorka S, Keller W (2011). "The structure of bacterial S-layer proteins". Molecular Assembly in Natural and Engineered Systems. Progress in Molecular Biology and Translational Science. Vol. 103. pp. 73–130. doi:10.1016/B978-0-12-415906-8.00004-2. ISBN   9780124159068. PMID   21999995.{{cite book}}: |journal= ignored (help)
  20. ↑ Houwink, AL (1953). "A macromolecular mono-layer in the cell wall of Spirillum spec". Biochim Biophys Acta. 10 (3): 360–6. doi:10.1016/0006-3002(53)90266-2. PMID   13058992.
  21. ↑ 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. Bibcode:2012PNAS..10911812A. doi: 10.1073/pnas.1120595109 . PMC   3406845 . PMID   22753492.
  22. ↑ 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" (PDF). Nature. 487 (7405): 119–22. Bibcode:2012Natur.487..119B. doi:10.1038/nature11155. PMID   22722836. S2CID   4389187.
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  25. ↑ Pum D, Sleytr UB (2014). "Reassembly of S-layer proteins". Nanotechnology. 25 (31): 312001. Bibcode:2014Nanot..25E2001P. doi:10.1088/0957-4484/25/31/312001. PMID   25030207. S2CID   39889746.
  26. ↑ Chung S, Shin SH, Bertozzi CR, De Yoreo JJ (2010). "Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics". Proc. Natl. Acad. Sci. USA. 107 (38): 16536–16541. Bibcode:2010PNAS..10716536C. doi: 10.1073/pnas.1008280107 . PMC   2944705 . PMID   20823255.
  27. ↑ Shin SH, Chung S, Sanii B, Comolli LR, Bertozzi CR, De Yoreo JJ (2012). "Direct observation of kinetic traps associated with structural transformations leading to multiple pathways of S-layer assembly". Proc. Natl. Acad. Sci. USA. 109 (32): 12968–12973. Bibcode:2012PNAS..10912968S. doi: 10.1073/pnas.1201504109 . PMC   3420203 . PMID   22822216.
  28. ↑ Ilk N, Egelseer EM, Sleytr UB (2011). "S-layer fusion proteins - construction principles and applications". Curr. Opin. Biotechnol. 22 (6): 824–831. doi:10.1016/j.copbio.2011.05.510. PMC   3271365 . PMID   21696943.
  29. ↑ Schuster B, Sleytr UB (2014). "Biomimetic interfaces based on S-layer proteins, lipid membranes and functional biomolecules". J. R. Soc. Interface. 11 (96): 20140232. doi:10.1098/rsif.2014.0232. PMC   4032536 . PMID   24812051.
  30. ↑ Schuster B, Sleytr UB (2021). "S-Layer Ultrafiltration Membranes". Membranes. 11 (4): 275. doi: 10.3390/membranes11040275 . PMC   8068369 . PMID   33918014.
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