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Stress factors such as an increase in temperature can lead to shedding of the bacteria from these carrier fish [ 40 ]. Basement membrane binding may be a factor in allowing the bacteria to persist in the host during this state. Mutagenesis of two genes encoding polytopic cytoplasmic membrane proteins, which are located downstream of the A. This mutant exhibits increased virulence when introduced intraperitoneally into rainbow trout. An asoB mutant was found to have S-layer subunit protein VapA present in the cytoplasmic membrane fraction and displayed reduced virulence when administered by immersion but not when introduced intraperitoneally [ 42 ].

This may indicate that the S-layer plays a role in early colonisation by A. These mutants demonstrate that there are a number of factors involved in the secretion and assembly of the S-layer, and that changes in the structural integrity of the S-layer can have significant effects on virulence. The S-layers of Aeromonas spp.

Basement membrane binding by the S-layer in organs such as the kidneys, where the bacteria are maintained in a carrier state, could allow persistence of the bacteria. Similarly, binding of the S-layer to soluble fibronectin, for example, could mask the cells from the immune response by sterically blocking immunogenic epitopes. There are significant differences between the role of the S-layer of A. Further research is required with isogenic mutants of a greater number of strains to determine the precise roles of the S-layers in bacteria from this diverse genus.

To date, the study of the S-layer of A. The continued study of Aeromonas S-layers will provide new insights into mechanisms of high-level gene expression and regulation, protein secretion, outer membrane biogenesis and mechanisms of pathogenesis. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide.

Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents. The synthesis, secretion and role in virulence of the paracrystalline surface protein layers of Aeromonas salmonicida and A. Oxford Academic. Google Scholar. Trevor J. V8W 3P6, Canada. Corresponding author.

Cite Citation. Permissions Icon Permissions. Abstract The S-layers of the Aeromonas spp. Aeromonas , S-layer , Virulence , Secretion.

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Open in new tab Download slide. Negative stain of the tetragonal S-layer of A. Effect of S-layer mutations on virulence in A. Open in new tab. Search ADS. Mesophilic aeromonads in human disease: current taxonomy, laboratory identification and infectious disease spectrum. Recent advances in the study of the taxonomy, pathogenicity and infectious syndromes associated with the genus Aeromonas.

Purification and disposition of a surface protein associated with virulence of Aeromonas salmonicida. Virulence markers of mesophilic aeromonads: association of the autoaggluttination phenomenon with mouse pathogenicity and the presence of a peripheral cell-associated layer. Immunochemical analysis and possible biological role of an Aeromonas hydrophila surface array protein in septicemia.

Messner, P. Academic Press, London. Trust, T. Beveridge, T. Plenum Publishing Corporation, New York. Two patterns in the Aeromonas salmonicida A-layer may reflect a structural transformation that alters permeability. Three-dimensional structure of the crystalline surface layer from Aeromonas hydrophila.

Structure of an S-layer on a pathogenic strain of Aeromonas hydrophila. Three dimensional structure of the surface layer from the fish pathogen Aeromonas salmonicida. Roles of structural domains in the morphology and surface anchoring of the tetragonal paracrystalline array of Aeromonas hydrophila. The association of the surface array and the outer membrane of Deinococcus radiodurans. Synthesis, export, and assembly of Aeromonas salmonicida A-layer analyzed by transposon mutagenesis.

Surface protein composition of Aeromonas hydrophila virulent for fish: identification of an S-layer protein. Cloning of the gene for the surface array protein of Aeromonas salmonicida and evidence linking loss of expression with genetic deletion. Structure of the tetragonal surface virulence array protein and gene of Aeromonas salmonicida.

Tyrosine phosphorylation of the tetragonal paracrystalline array of Aeromonas hydrophila : molecular cloning and high-level expression of the S-layer protein gene. Isolation and biochemical characterization of the S-layer protein from a pathogenic strain of Aeromonas hydrophila. Transcriptional analysis of the Aeromonas salmonicida S-layer protein gene vap A. The leucine zipper of Aeromonas salmonicida AbcA is required for the transcriptional activation of the P2 promoter of the surface layer structural gene, vapA , in Escherichia coli. Expression, secretion and antigenic variation of bacterial S-layer proteins.

The Aeromonas hydrophila exeE gene, required both for protein secretion and normal outer membrane biogenesis, is a member of a general secretion pathway. Isolation and analysis of eight exe genes and their involvement in extracellular protein secretion and outer membrane assembly in Aeromonas hydrophila.

Cloning and study of the genetic organization of the exe cluster of Aeromonas salmonicida. Molecular analysis of an A-protein secretion mutant of Aeromonas salmonicida reveals a surface layer-specific protein secretion pathway. A specific PulD homolog is required for the secretion of paracrystalline surface array subunits in Aeromonas hydrophila. Novel structural patterns in divalent cation-depleted surface layers of Aeromonas salmonicida. Loss of virulence during culture of Aeromonas salmonicida at high temperature.

Thomas, S. Role of surface components in serum resistance of virulent Aeromonas salmonicida. Antigenic diversity of S-layer proteins from pathogenic strains of Aeromonas hydrophila and Aeromonas sobria. High-affinity binding of the basement membrane protein collagen type IV to the crystalline virulence surface protein array of Aeromonas salmonicida.

Binding of laminen and fibronectin by the trypsin-resistant major structural domain of the crystalline virulence surface array protein of Aeromonas salmonicida. Plenum Press, New York. Molecular characterization of an Aeromonas salmonicida mutant with altered surface morphology and increased systemic virulence. An Aeromonas salmonicida gene required for the establishment of infection in rainbow trout Oncorhynchus mykiss. Detection of Aeromonas salmonicida from fish by using polymerase chain reaction amplification of the virulence surface array protein gene. Surface-disorganized, attenuated mutants of Aeromonas salmonicida as furunculosis live vaccines.

Recombinant infectious hematopoietic necrosis virus and viral hemorrhagic septicemia virus glycoprotein epitopes expressed in Aeromonas salmonicida induce protective immunity in rainbow trout Oncorhynchus mykiss.

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Published by Elsevier Science B. The threshold for the transition between native and non-native S-layer parameters was four methylene groups. Finally, it must be noted that different lattice constants were observed on the two surfaces. It was confirmed that electrostatic interactions COOH functional groups induce a faster adsorption than hydrophobic CH 3 groups or hydrophilic OH groups interactions — as already shown for the reattachment on the bacterial cell Sleytr, ; Mader et al. As required by technological demands, a great variety of supports, differing in their physico-chemical properties, are currently investigated.

Silicon and metal surfaces are exploited for applications in nano-electronics, glasses in nano-optics, and polymeric surfaces, such as epoxy-based negative photoresists e. SU-8 , in microfluidics Picher et al. For example, silanization with either aminopropyltriethoxysilane or octadecyltrichlorosilane is often used in such applications to render the properties of a glass surface hydrophobic Lopez et al.

AFM and Quartz Crystal Microbalance with Dissipation monitoring QCM-D studies demonstrated that the S-layer protein SbpA adsorbs on aminopropyltriethoxysilane- and octadecyltrichlorosilane-modified surfaces much faster than on the native silicon dioxide rendered hydrophilic by plasma treatment Lopez et al. AFM measurements showed that the crystalline domains were much smaller on silanized substrates compared with hydrophilic silicon dioxide ones.

The protein adsorption was diffusion controlled up to a threshold concentration of 0. However, with respect to the reassembly of S-layer proteins per se at such interfaces, a detailed study using the S-layer protein SbpA as model system had been carried out on solid-supported lipid bilayers Chung et al. The reassembly of the square lattice followed a multistage, nonclassical pathway in which monomers, with extended conformation, first formed a mobile adsorbed phase from which they condensed into amorphous clusters.

In a subsequent phase transition, the S-layer proteins folded into clusters of compact tetramers. In the following, crystal growth proceeded by the formation of new tetramers exclusively at cluster edges. In the mid-eighties, first reports on cloning and sequencing of S-layer genes were published. The first complete S-layer gene sequence was that for the outer wall protein OWP from Bacillus brevis 47 Tsuboi et al. With the accumulation of S-layer gene sequences, screening for putative sequence identities became possible. Although S-layer proteins show low homology on the sequence level, common structural organization principles have been identified.

The elucidation of the structure—function relationship of distinct segments of S-layer proteins started with the production of N- and C-terminally truncated forms which were used for recrystallization and binding studies Jarosch et al. Thereby, it turned out that S-layer proteins exhibit mostly two separated morphological regions: one responsible for cell wall binding and the other required for self-assembly. The position of the cell wall-anchoring region within the protein can vary between bacterial species.

Studies on a great variety of S-layer proteins from Bacillaceae revealed the existence of specific binding domains on the N-terminal part for sugar polymers, so-called secondary cell wall polymers SCWPs , which are covalently linked to the peptidoglycan of the cell wall Egelseer et al. This specific molecular interaction is often mediated by a recurring structural motif of approximately 55 amino acids, which is mostly found in triplicate at the N-terminus of S-layer proteins.

These so-called S-layer homology SLH motifs are involved in cell wall anchoring of S-layer proteins by recognizing a distinct type of SCWP, which carries pyruvic acid residues Ries et al. The need for pyruvylation was confirmed by the construction of knock-out mutants in Bacillus anthracis and Thermus thermophilus Mesnage et al. The strong correlation between the existence of SLH motifs and the presence of the gene for the pyruvyltransferase CsaB was demonstrated once again in a very recent study Pleschberger et al. The two ORFs encoding the autolysin rAbpA and the pyruvyl transferase rCsaB were cloned and expressed in Escherichia coli , and the recombinantly produced proteins were characterized regarding their secondary structure and their enzymatic activity Pleschberger et al.

Recently, the role of the three SLH motifs in the glycosylated S-layer protein SpaA of Paenibacillus alvei CCM T was analyzed by site-directed mutagenesis and visualization by in vivo studies using homologous expression as well as in vitro binding assays Janesch et al. It was demonstrated that the SLH motifs of SpaA are sufficient for in vivo cell surface display of foreign proteins at the cell surface of P.

Furthermore, it was shown that in P. Using affinity studies and SPR spectroscopy, a further main type of binding mechanism was described for G. Among the S-layer proteins from Lactobacilli, which are devoid of SLH motifs, the regions important for cell wall binding and self-assembly are quite different. In the S-layer proteins SlpA of Lactobacillus acidophilus and CbsA of Lactobacillus crispatus , a putative carbohydrate-binding repeat comprising approximately the last C-terminal amino acids has been identified.

This is one-third of this S-layer protein and was suggested to be involved in cell wall binding Smit et al. However, contrary to the L. In Gram-negative bacteria, no general S-layer-anchoring motif has been identified and the S-layer is attached with its N- or C-terminus to the lipopolysaccharide component of the outer membrane Thomas et al.

For the Caulobacter crescentus S-layer protein RsaA, recrystallization on lipid vesicles was obtained only when the vesicles contained the specific species of Caulobacter smooth lipopolysaccharide that previous studies implicated as a requirement for attaching the S-layer to the cell surface Nomellini et al. The specific type of phospholipids did not appear critical; phospholipids rather different from those present in Caulobacter membranes or archaeal ether lipids worked equally well.

However, the source of lipopolysaccharide was critical. Furthermore, efficient recrystallization and long range order could not be obtained with pure protein, although it was apparent that calcium was required for crystallization Nomellini et al. Using selected N- or C-terminally truncated S-layer protein forms as fusion partners for foreign proteins or domains, it turned out that S-layer proteins are able to assemble into geometrically highly defined layers while incorporating a segment that has never participated in lattice formation.

To date, a great variety of functional, chimeric S-layer proteins is available Fig. Functional recombinant S-layer fusion proteins and their applications modified after; Sleytr et al. Schematic drawings of mono- and oligomeric S-layer fusion proteins: a fusion protein with single function, b fusion protein acting as template for oligomeric assemblies, c functional domains bound via flexible linkers to S-layer proteins assemble on the surface of the S-layer lattice.

Although considerable knowledge has already been experimentally accumulated on the structure, biochemistry, assembly characteristics, and genetics of S-layer proteins, no structural model at atomic resolution was available for quite a while. Therefore, neither their tertiary structure nor exact amino acid or domain allocations in the lattices were known. A first tertiary structure prediction for an S-layer protein SbsB from G.

For the simulation of the folding, SbsB was divided into eight structurally independent domains: three domains at the N-terminus and five domains at the C-terminus. The C-terminus of SbsB accounts for the main part of the protein. Molecular dynamics MD simulations performed for 30 ns in vacuum finally led to three main domains at the C-terminal end.

The first domain is linear aa —aa and connects the N-terminus with the L-shaped part of the C-terminus, which is made up of the other two domains aa —aa and aa —aa which are fibronectin type III and Ig-like group 2 domains, respectively. Later on, the same theoretical approach was used to predict the 3D structure of SbpA from L. The first high-resolution structure of a domain of a bacterial S-layer protein was obtained from X-ray studies with an assembly-negative, water-soluble, truncated form of the S-layer protein SbsC of G.

Despite the intrinsic property of S-layer proteins to reassemble solely in two dimensions, it turned out that this truncated form is well suited for 3D crystallization studies. The crystal structure of rSbsC 31— P2 1 space group symmetry revealed a novel fold, consisting of six separate domains, which are connected by short flexible linkers. To complete the structure of the full-length protein, additional soluble constructs containing the crucial domains for self-assembly were cloned, expressed, and purified Dordic et al.

Currently, rebuilding and refinement of the structure is in progress and upon completion will yield the complete structure of the full-length SbsC protein. Most recently, the full-length atomistic SbsB structure was solved by the use of nanobody-aided crystallization Baranova et al. It is interesting to see that the choice of structurally meaningful parts and domain predictions used in the theoretical approach ]described before Horejs et al.

However, the first reported crystal structure of an S-layer protein from a bacterial pathogen was described for Clostridium difficile Fagan et al. The crystal structure of a truncated derivative of the LMW protein was resolved down to 2. The first high-resolution crystal structure of an archaeal S-layer protein 2. In the past few years, substantial progress has been made in describing the archaeal N -glycosylation pathway, where the glycan is linked to asparagine.

For many years, due to the lack of suitable molecular tools, the understanding of the genetic basis for S-layer protein glycosylation was lagging behind the structural analyses. An important milestone was reached with the identification of the first S-layer glycosylation slg gene cluster in the bacterium G.

Until now, about 15 different S-layer glycoprotein glycan structures have been fully or partially elucidated, and several slg gene clusters have been identified, sequenced, and characterized Ristl et al. In a proof-of-concept study, the transfer of the Campylobacter jejuni heptasaccharide and the E. The degree of glycosylation of the S-layer neoglycoproteins after purification from the periplasmic fraction reached completeness and electron microscopical investigations revealed that recombinant glycosylation is fully compatible with the S-layer protein self-assembly system Steiner et al.

Based on the fact that the two Bacteroidales species Bacteroides fragilis and Tannerella forsythia both have general O -glycosylation systems and share a common glycosylation sequon, a very recent study reports on the successful transfer of the B. To conclude, the S-layer system is a promising strategy for multivalent glycan display approaches where strict nanometer-scale control over position and orientation of the glycan epitopes is desired.

When other cell surface components e. As S-layer carrying Bacteria and Archaea are ubiquitous in the biosphere, the supramolecular concept of a closed, isoporous protein lattice represent specific adaptations to diverse environmental and ecological conditions. Most important, S-layers are generally part of complex envelope structures Fig. Several of the functions assigned to S-layers are still hypothetical and not based on firm experimental data.

This assumption was addressed in detail by studying the role of the S-layer in morphogenesis and cell division of the rod shaped T. In this context, data obtained on cell surface hydrophobicity of a collection of different Lactobacillus strains with and without S-layers have to be taken into account. Interestingly, cell adhesion of the S-layer carrying strain G. For the latter, hydrophobic interaction chromatography revealed a more pronounced hydrophilic surface. In the case of the pathogenic organism Aeromonas salmonicida , it could be demonstrated that the presence of the S-layer makes the cell surface much more hydrophobic Trust et al.

S-layers are capable of interacting with particles and materials of different physiochemical properties, thereby favoring adherence of whole cells to solid surfaces. Furthermore, S-layers have been suggested to fulfill a protective function for the living cells by excluding hostile lytic enzymes such as muramidases and proteases. However, this could only be confirmed for a few examples. The S-layer from Sporosarcina urea was found to protect the murein sacculus from lysozyme attack, possibly due to the presence of pores smaller than the enzyme molecules Beveridge, S-layers from Gram-negative Bacteria such as A.

More recently experimental data were presented which indicate that the S-layer that covers the outer membrane of C. A quite interesting type of protective function was reported for the S-layer lattice of Synechococcus Schultze-Lam et al. The hexagonally ordered S-layer lattice functions as a template for fine-grain mineralization and is continuously shed from the cell surface to get rid of mineral depositions thereby maintaining basic vital processes such as growth and division as well as nutrient transport.

S-layers can contribute to virulence when they are present as a structural component of the cell envelope of pathogens. Bacillus anthracis , the etiological agent of anthrax, is capable of lethality in both animals and humans and is a biothreat of great concern Blendon et al. The surface of B. Two proteins, Sap Surface array protein and EA1 Extractable Antigen 1 , encoded by the clustered chromosomal genes sap and eag , are the S-layer components Etienne-Toumelin et al.

Both proteins have an N-terminal cell wall-anchoring domain consisting of three SLH motifs followed by a putative crystallization domain comprising C-terminal amino acids Mesnage et al. During the exponential growth phase, B. Immunoreactivity studies using a truncated S-layer protein form devoid of the SLH moiety indicated that the C-terminal segment contributes significantly to S-layer immunogenicity Ariel et al. In a recent study, single domain antibodies sdAbs were isolated using a phage display library prepared from immunized llamas Walper et al.

Interestingly, the protein target for all six sdAb families was determined to be the S-layer protein EA1, which is present in both vegetative cells and bacterial spores. This research demonstrates the capabilities of these sdAbs and their potential for integration into current and developing assays and biosensors Walper et al. Also recently, evidence was provided that B.

This finding suggests that the Isd system can receive heme from multiple inputs and may reflect an adaptation of B. Understanding the mechanism of heme uptake in pathogenic Bacteria is important for the development of novel therapeutics to prevent and treat bacterial infections Tarlovsky et al. Bacillus cereus G is the causative agent of respiratory anthrax-like disease in humans, which is most frequently observed in welders Callahan et al.

In a very recent study, Wang et al. The finding that B. One of these functions is the control of the chain length of vegetative forms which represents a mechanism for bacterial escape from opsonophagocytic killing. If bacillus chain length exceeds the size of macrophages or granulocytes, Bacteria cannot be engulfed Wang et al.

The C. S-layer proteins could mediate the binding to both the intestinal epithelial cells and some components of their extracellular matrix fibers, contributing to further tissue damage Calabi et al. Evidence was provided that the HMW subunit functions as an adhesin which mediates adherence of C. Ausiello and coworkers demonstrated the ability of C. Host antibody response plays an important role in protection, in particular IgM anti-S-layer proteins have been associated with a reduced risk of recurrent C.

In this context, a protective effect of anti-S-layer protein serum has also been observed in a lethal hamster challenge model. The potential mechanism of action of the antiserum was shown to be through enhancement of C. Therefore, the possible use of S-layer proteins in a multicomponent vaccine against C. It is now evident that Lactobacilli over a long evolutionary period have colonized the mucosa of the upper gastrointestinal tract and the vagina coexisting in mutualistic relationship with the host.

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With L. As individual strains of immunomodulatory probiotic Bacteria e. Campylobacter fetus , a spiral Gram-negative bacterium, is a recognized pathogen of cattle and sheep that can also infect humans Guerrant et al. Campylobacter fetus may be either type A or type B based on serotype, lipopolysaccharide structure, and S-layer protein type Dubreuil et al.

The S-layer proteins have been shown to play a critical role in C. Graham and coworkers showed that attachment to extracellular matrix components EMC was neither correlated with S-layer expression nor with cell surface hydrophobicity Graham et al. However, ligand immunoblots, identified the S-layer protein as a major site of fibronectin binding, and modified ECM binding assays revealed that soluble fibronectin significantly enhanced the attachment of S-layer-expressing C.

Native S-layer containers were composed of three adjacent layers namely the S-layer, the peptidoglycan-containing layer, and an inner S-layer attached to the inner face of the peptidoglycan layer. The latter was formed upon removal of the plasma membrane out of the pool of S-layer subunits originally entrapped in the peptidoglycan layer Breitwieser et al. To distinguish between the molecular sieving properties between the S-layer and the peptidoglycan layer, the peptidoglycan layer was digested with lysozyme.

The solutions selected for the molecular sieving measurements were sugars, proteins, and dextrans of increasing molecular weights. It was clearly demonstrated that the S-layer lattices allow free passage for molecules with a molecular weight of up to 30 kD and showed sharp exclusion limits between molecular weights of 30 and 45 kD, suggesting a limiting pore diameter in the range of 3—4.

Moreover, of great relevance in these studies was the observation that the peptidoglycan layer does not limit the passage of molecules capable of penetrating the S-layer. Most important a great variety of permeability studies on S-layers from Bacillaceae demonstrated that the surface and pore areas of the protein meshwork have a very low tendency for unspecific adsorption of macro molecules Sleytr et al.

This characteristic of S-layers is seen essential for maintaining an unhindered exchange of nutrients and metabolites between the cell and its environment. In this context, it is also important to note that the S-layer in Gram-positive Bacteria masks the net negative charge of the peptidoglycan layer which significantly determines interactions between living cells and its environment. The bacterial cell wall plays a key role in the exchange of substrates between the bacterium and its surrounding environment.

Because S-layer-carrying G. It was also suggested that S-layers from members of the family Bacillaceae could delineate a kind of periplasmic space in cell envelopes of Gram-positive organisms and consequently delay or control the release of exoenzymes Graham et al. Binding to the cell surface has also been reported for exoenzymes and exoproteins including the outer layer proteins OlpA and OlpB of Clostridium thermocellum Fujino et al.

First studies concerning the importance of the S-layer lattice with regard to exoprotein secretion were carried out with the exoamylase-producing strain G. Affinity experiments strongly suggested the presence of a specific recognition mechanism between the amylase molecules and S-layer protein domains either exposed on the outermost surface or inside the pores Egelseer et al. On starch medium, both strains of G. Using heterologously produced N- or C-terminally truncated SbsC forms and the native HMMA for affinity studies, it turned out that the N-terminal part of SbsC must comprise the binding region for the exoenzyme Jarosch et al.

On the basis of all available data, a specific binding region for each of the three cell wall components rSbsC, SCWP, and peptidoglycan could be identified in the C-terminal part of the rHMMA, representing the smallest regions necessary for interaction Ferner-Ortner-Bleckmann et al.

For G. During the oxygen-induced switch from the wild-type strain G. However, in all variants investigated so far, the peptidoglycan-chemotype remained constant. In order to adapt to any change in the composition of the cell wall induced by altered environmental conditions and variant formation, the HMMA evolved a multifunctional binding mechanism that provides the enzyme with a great flexibility. S-layers are a very common surface structure in Bacteria including Cyanobacteria Smarda et al. A unique ecological role could be demonstrated for the cyanobacterial S-layer of Synechococcus strain GL The S-layer has a hexagonal monomer arrangement and provides regularly spaced, chemically identical nucleation sites for mineral growth Schultze-Lam et al.

Eventually, the S-layer becomes encrusted with mineral and is shed so that cells have a patchy appearance with respect to the location of mineralized portions of their surface. Shedding of S-layer material could be a common process of Bacteria to get rid of mineral depositions on their cell surface thereby maintaining basic vital processes such as growth and division as well as nutrient transport.

The natural pH value of the lake c. Although the involvement of cyanobacteria in the formation of calcium carbonate has been well established, microbial involvement in the formation of other carbonate minerals has not been extensively studied. Due to the difficulty of examining the process of calcite nucleation on natural matrices such as Synechococcus S-layers, a very recent review focused on studies of nucleation at carboxyl-terminated alkane thiol SAM surfaces on noble metal substrates.

The ability to form fine-grain mineral sediments may be much more common among planktonic prokaryotes endowed with S-layers than can be imagined currently Klingl et al. Because prokaryotes exist since approximately 3. Currently, there is much interest in the synthesis of inorganic materials using biomimetic approaches. For that purpose, the S-layer protein SbpA of L. Studying the formation of silicified S-layers may help to develop novel silicon-based materials with enhanced mechanical stability and optical properties Schuster et al.

Another current approach considers the use of bacterial S-layers as a potential alternative for bioremediation processes of heavy metals in field. In , a recombinant bioremediation agent of high efficiency and low cost was developed by inserting a hexa-histidine peptide into a permissive site of the S-layer protein RsaA of the harmless, Gram-negative bacterium C. To summarize, these special capabilities of the bacterial cells and their S-layers are highly interesting for the clean-up of contaminated waste waters, for the recovery of precious metals from wastes of the electronic industry, as well as for the production of metal nanoclusters.

S-layer ultrafiltration membranes SUMs were produced by depositing S-layer fragments as a coherent layer on microfiltration membranes. The mechanical and chemical stability of their composite structure is subsequently obtained by inter- and intramolecular cross-linking. The chemical and thermal resistance of these membranes was shown to be comparable to polyamide membranes. The uniformity of functional groups on both the surface and within the pore area of the S-layer lattice could be used for very accurate chemical modifications in the subnanometer range.

In this way, depending on the specific separation processes, SUMs can be prepared with different net charges, hydrophilic or hydrophobic surface properties and separation characteristics. Most important for separation processes, in comparison with conventional ultrafiltration membranes produced by amorphous polymers, SUMs revealed an extremely low unspecific protein adsorption membrane fouling in buffer solutions. Because of their high stability under shear forces, SUMs have also a broad application potential as a matrix for immobilizing functional molecules e.

Because S-layer lattices are composed of identical protein or glycoprotein species, functional sequences introduced either by chemical modification or genetic engineering must be aligned in exact positions and orientation down to the subnanometer scale Sleytr et al. Chemical modification and labeling experiments revealed that S-layer lattices possess a high density of functional groups on the outermost surface. Furthermore, a universal biospecific matrix for immunoassays and dipsticks could be generated by immobilizing monolayers of either protein A or streptavidin onto SUMs Breitwieser et al.

SUMs were also chosen as matrix for an amperometric glucose sensor using glucose oxidase as the biologically active component Neubauer et al. Just recently, a lab-on-a-chip containing embedded amperometric sensors that are coated with crystalline monolayers formed by the S-layer protein SbpA of L. This novel combination of biologically derived nanostructured surfaces with microchip technology constitutes a powerful new tool for multiplexed analysis of complex samples.

Several studies already demonstrated that preformed nanoparticles can be bound in regular distribution on native S-layers Hall et al. The pattern of bound molecules and nanoparticles reflected the size of the morphological units, the lattice symmetry, and the physicochemical properties of the array.

Using electron microscopical methods, the distribution of net negatively charged domains on S-layers could be visualized after labeling with the positively charged topographical marker polycationic ferritin Messner et al. Due to the promising results obtained with native S-layers as immobilization matrix, genetic engineering of S-layer proteins was envisaged. It turned out that S-layer proteins are capable of tolerating fusions with foreign proteins or domains that have never participated in lattice formation while retaining the ability to assemble into geometrically highly defined layers.

To date, a great variety of functional S-layer fusion proteins was cloned and heterologously expressed in E. Using TEM and AFM as well as functional tests, it could be demonstrated that the recrystallization properties conferred by the S-layer protein moiety as well as the functionalities of the fused peptide sequences were retained in all S-layer fusion proteins. Moreover, functional proteins maintain their functionality much better on the S-layer protein matrix in comparison when being directly attached immobilized to solid supports.

S-layer fusion proteins incorporating either the sequence of the hypervariable region of heavy chain camel antibodies recognizing lysozyme or the prostate-specific antigen PSA; Pleschberger et al. Significant advantages for enzyme immobilization by the S-layer self-assembly system over processes based on random immobilization of sole enzymes include the requirement of only a simple, one-step incubation process for site-directed immobilization without preceding surface activation of the support. Moreover, the provision of a cushion for the enzyme through the S-layer moiety of the fusion protein prevents denaturation and consequently loss of enzyme activity upon immobilization.

In a recent study, for the first time, self-assembling biocatalysts, consisting of S-layer lattices exhibiting surface exposed active multimeric extremozymes, were produced Fig. The challenging step forward was to use enzymes of extremophiles which are active only in the multimeric state. For proof of concept, the tetrameric enzyme xylose isomerase and the trimeric enzyme carbonic anhydrase were selected and fused via a peptide linker to the C-terminal end of the S-layer protein SbpA of L. The study demonstrated that the outstanding robustness and high stability of multimeric extremozymes could be combined with the unique lattice forming capability and periodicity of bacterial S-layers, thereby providing a matrix for a most accurate spatial presentation of the multimeric enzymes Ferner-Ortner-Bleckmann et al.

Core streptavidin was either fused to N- or C-terminal positions of S-layer proteins. As biologically active streptavidin occurs as tetramer, functional heterotetramers consisting of one chain fusion protein and three chains of core streptavidin were prepared by applying a special refolding procedure Moll et al. For that purpose, S-layer proteins are prime candidates for vaccine development. Because a reproducible immobilization of peptide epitopes to common carriers which were used as monomers in solution or as dispersions of unstructured aggregates on aluminum salts could not be achieved Brown et al.

Therefore, several conjugate vaccines with S-layer glyco proteins and carbohydrate antigens poly- and oligosaccharides , haptens or the recombinant birch pollen allergen Bet v1 were produced which showed promising results in vaccination trials Sleytr et al. In earlier studies, the crystalline surface-layer glycoproteins of T. The haptens were immobilized to either the protein moiety or the glycan chains of the respective S-layer glycoproteins. Immunization of mice with conjugates of oligosaccharide haptens and crystalline S-layers primed the animals for a strong, hapten-specific, delayed-type hypersensitivity DTH response Smith et al.

Apparently, the natural assembly of S-layer proteins into large, two-dimensional arrays endows them with intrinsic adjuvant properties Smith et al. First studies concerning the applicability of S-layers as vaccine carrier for treatment of type I allergy were carried out using native or cross-linked S-layer self-assembly products and cell wall preparations from L. In a subsequent study, the adjuvant effect of S-layer proteins mediated by IL was demonstrated Jahn-Schmid et al.

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In the following years, chemical coupling procedures were replaced by genetic fusion of the major birch pollen allergen Bet v1 to bacterial S-layer proteins resulting in recombinant fusion proteins exhibiting reduced allergenicity as well as immunomodulatory capacity Breitwieser et al. In vitro cell culture studies showed that S-layer coated emulsomes can be taken up by human liver carcinoma cells HepG2 without any significant cytotoxicity.

S-layer coating led to a change in the zeta potential of the emulsomes from positive to negative, thus protecting the cell from oxidative stress and cell membrane damage. Bacillus anthracis spores germinate to vegetative forms in host cells and produce fatal toxins. In a former study, a recombinant B. The immune response to ToxC was sufficient to protect mice against tetanus toxin challenge and could be tested for the development of new live veterinary vaccines Mesnage et al.

Figure 10 from Advances in Bacterial Paracrystalline Surface Layers - Semantic Scholar

In a very recent study, the protective effect of EA1 against anthrax was investigated Uchida et al. For that purpose, mice were intranasally immunized with recombinant EA1, followed by a lethal challenge of B. It could be demonstrated that immunization with EA1 greatly reduced the number of bacteria in infected organs and protected the mice from lethal infection, thus suggesting that EA1 is a novel candidate for an anthrax vaccine.

The display of heterologous proteins on the cell surface of lactic acid bacteria LAB is an exciting and emerging research area that holds great promise for the developments of live vaccine delivery system. Small model peptides have already been displayed in each monomer of the S-layer of L. A recent study describes a novel characteristic of the S-layer of L. The S-layer protein of this strain was shown to bind electrostatically to dendritic cell-specific ICAMgrabbing nonintegrin DC-SIGN , a cell surface adhesion factor that enhances viral entry of several virus families including HIV type 1, hepatitis C virus, Ebola virus, cytomegalovirus, Dengue virus, and SARS coronavirus and may therefore be applied as novel antiviral agent Martinez et al.

One of the greatest obstacles in developing an effective vaccine against Aeromonas hydrophila , an important fish pathogen in aquaculture systems, is its high heterogeneity in nature Poobalane et al. The results of the study suggested that the recombinant S-layer protein of A. The S-layer proteins of C.

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Some years ago, O'Brien and coworkers showed that a passive immunization using anti-S-layer protein antibodies significantly delayed the progress of C. In a subsequent study, C. However, none of the regimes tested conferred complete protection of animals and antibody stimulation was variable and generally modest or poor Ni Eidhin et al. In a recent, novel approach, the C. Hamster immunization studies demonstrated that Cwp84 is an attractive component for inclusion in a vaccine to reduce C. The building principle of S-layer supported lipid membranes SsLMs is copied from the supramolecular cell envelope structure of Archaea Fig.

Hence, S-layers must therefore integrate the basic functions of mechanical and osmotic cell stabilization Engelhardt, As suitable methods for disintegration of archaeal S-layer protein lattices and their reassembly into monomolecular arrays on lipid films are not yet available, S-layer proteins from Gram-positive Bacteria are used for the generation of SsLMs Schuster et al. Disregarding emulsomes, these model lipid membranes consist either of an artificial phospholipid bilayer or a tetraetherlipid monolayer which replaces the cytoplasmic membrane and a closely associated bacterial S-layer lattice Fig.

In addition, a second S-layer acting as protective molecular sieve and further stabilizing scaffold and antifouling layer can be recrystallized on the top of the previously generated SsLM Fig. Some head groups of the lipid molecules within the membrane gray interact electrostatically with certain domains on the S-layer lattice. A further glyco protein S-layer lattice can be recrystallized on the outer leaflet of the lipid membrane left. In analogy, some head groups of the lipid molecules within the membrane gray interact electrostatically with certain domains of the S-layer proteins.

The lipid molecules on the left side depict schematically phospholipids, whereas the lipid molecules on the right side indicate ether lipids. SsLMs have attracted lively interest because of three main reasons: First, they constitute a versatile biomimetic model to study the characteristics of the archaeal cell envelope by a broad arsenal of surface-sensitive techniques and sophisticated microscopical methods.

Second, with SsLMs, surfaces with new properties such as an antifouling characteristics for application in material science and nanomedicine can be generated. Thus, SsLMs received widespread recognition in drug discovery and protein—ligand screening. Formation of S-layer lattices covering the entire area of lipid films has been observed on zwitterionic phospholipids such as phosphatidyl cholines and in particular phosphatidyl ethanolamines, but not on negatively charged phospholipids Fig.

Most important, although peptide side groups of the S-layer protein interpenetrate the phospholipid head group regions almost in its entire depth, no impact on the hydrophobic lipid alkyl chains has been observed Schuster et al. To enhance the stability of the composite SsLMs, head groups of phospholipids have been covalently linked to the S-layer lattice Schrems et al. Interestingly, it became evident that in nature, archaeal S-layer proteins are targeted for post-translational modifications such as the addition of a lipid Kikuchi et al.

Hence, our approach to link lipids covalently to S-layer proteins is a biomimetic one as lipid modifications of S-layer glycoproteins are a general property of, for example, halophilic Archaea. SsLMs revealed a higher structural integrity when the pressure was applied from the S-layer faced side compared with plain bilayer lipid membranes BLMs.

A very important feature of supported lipid membranes is to preserve a high degree of mobility of the lipid molecules within the membrane fluidity and at the same time exhibiting sound condition of the overall membrane structure longevity. Moreover, the longevity of a tetraetherlipid monolayer sandwiched by an S-layer lattice on each side revealed in comparison with other approaches e.

This finding reflects also the optimization of the archaeal cell envelope structure by nature over billions of years. Lipid membranes generated on a porous support combine the advantage of easy manual handling, individual excess to both membrane surfaces, and possessing an essentially unlimited ionic reservoir on each side of the BLM. The surface properties of porous supports, such as roughness or great variations in pore size, have significantly impaired the stability of attached BLMs Nikolelis et al.

The life time could be even significantly increased to approximately 1 day forming an S-layer—lipid membrane—S-layer sandwich-like structure on SUMs Fig. Hence, the nanopatterned anchoring of lipids is a promising strategy for generating stable and fluid supported lipid membranes. Summary of membrane-active peptides and transmembrane proteins reconstituted in S-layer supported lipid membranes. A recent study showed that the S-layer lattice of C. Thus, the protection against APMs was proposed to be one biological function of S-layer lattices. In addition, this result confirmed the existence of a closed S-layer lattice without any defects tightly attached to the BLM.

Sulfolobicins, produced by several Sulfolobus strains, are an example for the interaction of proteinaceous toxins with S-layer proteins in nature. These toxins were found to be associated with cell-derived S-layer-coated vesicles resulting in no release of sulfolobicins in soluble form into the environment. These enzyme-containing vesicles of Sulfolobus islandicus, for example, were shown to kill cells of other strains of the same species Prangishvili et al.

In future, the ability to reconstitute integral membrane proteins in defined structures on, for example, sensor surfaces is one of the most important concerns in designing biomimetic sensing devices Nikolelis et al. Unilamellar liposomes are artificially prepared spherical containers comprising of a phospholipid bilayer shell and an aqueous core Bangham et al. In the latter, biologically active molecules such as hydrophilic drugs can be stored and transported, whereas the lipidic shell can be loaded with hydrophobic drugs. Emulsomes, however, are spherical systems with a solid fat core surrounded by phospholipid mono- and bilayer s Fig.

Hence, emulsomes show a much higher loading capacity for lipophilic drug molecules such as curcumin for targeted drug delivery to fight against cancer and other diseases Andresen et al. Furthermore, S-layer lattices as envelope structure covering the spherical containers Fig. When recrystallizing isolated S-layer subunits of Bacillaceae such as G. Coating of positively charged liposomes or emulsomes with bacterial S-layer fusion proteins resulted in inversion of the zeta potential from an initially positive value to a negative one Mader et al.

A similar behavior was observed for liposomes coated with S-layer proteins from Lactobacilli Hollmann et al. This finding supports the notion of the high stability of archaeal cell envelope structures. Moreover, to enhance the stability, the S-layer protein on the liposome can be cross-linked Schuster et al. In addition, cross-linking can also be utilized for covalent attachment of biologically relevant macromolecules Sleytr et al.

In turn, a layer of intact liposomes can also be reversibly tethered via the specific nickel—His-tag linkage on an S-layer lattice Kepplinger et al. Biotinylation of S-layer-coated liposomes resulted in two accessible biotin residues per S-layer subunit for subsequent streptavidin binding Mader et al. By this approach, biotinylated ferritin and biotinylated anti-human IgG were attached via streptavidin to S-layer-coated liposomes. An interesting approach is the recrystallization of the S-layer-enhanced green fluorescent protein EGFP fusion protein on liposomes Ilk et al.

The uptake of these specially coated liposomes by target cells and the functionality of transported drugs could be investigated simultaneously without the need of any additional labels. In vitro cell culture studies revealed that S-layer coated emulsomes can be up taken by HepG2 without showing any significant cytotoxicity. The utilization of S-layer fusion proteins equipped in a nanopatterned fashion by identical or diverse functions may lead to attractive nanobiotechnological and nanomedicinal applications, particularly as drug-targeting and delivery systems, as artificial virus envelopes in, for example, medicinal applications and in gene therapy Mader et al.

Regular arrays of macromolecules were first observed about 60 years ago in electron micrographs of prokaryotic cell wall fragments and were viewed originally as a curiosity. S-layers are now recognized as one of the most common envelope surface structures in Archaea and Bacteria. The widespread occurrence and the high physiological expense of S-layers raise the question of what selection advantage S-layer carrying organisms would have in their natural and frequently highly competitive habitats.

Moreover, if present, S-layers are also part of a more complex supramolecular envelope structure and consequently in functional terms must not be considered as isolated protein lattice. Defined domains of S-layer proteins have been identified as being involved in specific interactions with supporting cell envelope components. As S-layers are highly porous structures, some components of the supporting envelope layers such as side chains of lipopolysaccharides in Gram-negative bacteria; Chart et al. In functional terms, such complete cell surface modifications could prevent either attachment of specific phages or delay host immune reactions in case of pathogenic organisms.

So far no general biological function has been found, and many of the functions assigned to S-layers still remain hypothetical. As S-layers cover the surface of the whole cell as coherent layers, it has been inferred that many biological functions for the layer may depend on both the completeness of the covering and the structural and physicochemical repetitive uniformity down to the subnanometer scale Sleytr et al. A striking feature of many S-layers of Bacteria and Archaea is their excellent antifouling property.

Even when cells were harvested from complex environments or growth media containing a great variety of macromolecular components, the S-layer lattices were never masked by adsorbed molecules Fig. Obviously, the different electron microscopical preparation techniques retain deviations from the ideal crystal structure created by thermal lattice vibrations. These specific S-layer properties may additionally influence interactions with molecules in close proximity and consequently the observed antifouling properties.

Data derived from antifouling zwitterionic polymer coatings on composite nanofiltration membranes can lead to the conclusion that likewise the ultra-low fouling properties of S-layers may be affected by their zwitterionic surface properties Ji et al. In zwitterionic coatings developed for many applications that require biofouling resistance, ions alternate perfectly in the subnanometer scale between positive and negative charges preventing adsorption of naturally occurring molecules, particularly proteins.

Final proof for this hypothesis will depend on structural information of S-layer lattices at atomic resolution and detailed information on the impact of an S-layer surface on the molecular organization of the adjacent water boundary structure. Most recently, the unique antifouling properties of S-layers were successfully exploited for coating microfluidic channels in lab-on-a-chip devices Picher et al.

In addition to the unique physicochemical surface properties, the repetitive topographical characteristics of S-layers should be considered as relevant features affecting hydrodynamic surface properties of cells. It is tempting to speculate that the defined roughness of S-layer surfaces determines the flow resistance of cells in natural environments. Studies on friction flows of liquids at nanopatterned interfaces have shown that the slippage of fluids at channel boundaries is greatly increased using surfaces that are patterned on the nanometer scale Cottin-Bizonne et al. With prokaryotic organisms characterized by a large surface to volume ratio, such effects should be of particular importance.

Considering the combination of antifouling properties and increased slippage, the presence of S-layers may facilitate flagella-driven cell locomotion in natural habitats e. It will be interesting to see whether S-layer glycosylation even amplifies these important boundary conditions and surface properties.

We presume that besides the more specific functions identified for S-layers of different organisms e. Biomimetic approaches copying these unique S-layer surface properties could be of great technological relevance. In this context, it is of particular relevance to remember that in H. The first presumably corresponds to S-layer glycoprotein anchored to the membrane via the C-terminal transmembrane domain, whereas the other glycoprotein population is lipid-modified most presumably by archaetidic acid and associated with the membrane Kandiba et al.

Furthermore, S-layers as exclusive wall component in Archaea appear to be involved in maintaining of cell shape and in fission processes, but more detailed studies will be required to support this notion. Presumably, many recognized and predicted functions of bacterial S-layers, such as forming a barrier against predators, as molecular sieves that exclude hazardous components and retain useful molecules in the periplasmic space and as a promoter of very specific cell adhesion to surfaces and cells co-exist in different prokaryotic organisms.

Accumulated data on the structure, chemical composition, assembly, surface, and permeability properties have clearly shown that S-layers are the simplest biological glyco protein membranes which have developed during evolution. Most important, S-layer morphogenesis follows the theoretically simplest mechanism for a dynamic process of assembly of a closed container composed of monomolecular arrays of identical macromolecules. Moreover, S-layers have been shown to interact specifically with a great variety of amphiphilic molecules e.

It is even probable that structure—function relationships between S-layer lattices and virus capsids or animal and human virus envelopes exist Arbing et al. On the other hand, structures that look alike not necessarily have similar functions. The characteristic properties of S-layers, particularly their structural and physicochemical uniformity and the spontaneous association of constituent subunits under equilibrium conditions, have led to an astonishing spectrum of applications in nano bio technology, synthetic biology, and biomimetics Sleytr et al.

In this context, S-layer-carrying Lactobacilli as food grade and potentially probiotic organisms will gain importance for health-related applications such as live oral vaccines. S-layers are now recognized as versatile patterning elements for the generation of complex supramolecular structures involving other molecules such as lipids, proteins, glycans, and nucleic acids as well as inorganic materials e. This biomimetic approach, copying the supramolecular principle of cell envelopes of Archaea or envelopes of a great variety of viruses, allows stabilizing functional lipid membranes at the macroscopic scale.

Most recently, it could be demonstrated that S-layer stabilized lipid membranes can be functionalized by incorporating membrane proteins exploiting cell-free protein synthesis regimes E. Sinner, B. Schuster, S. Damiati, pers. Applications for S-layer neoglycoproteins concern receptor mimics, vaccine design, diagnostics, and drug delivery exploiting specific carbohydrate recognition Sleytr et al.

Although up to now the development of applied S-layer research has focused on life sciences, in future non-life science applications e. The total number of relevant publications currently more than on S-layers far surpasses the number of references that can be cited in this review. We therefore apologize to all those whose particular works were not cited here. FA and FA to D. National Center for Biotechnology Information , U. Fems Microbiology Reviews. Published online Feb Author information Article notes Copyright and License information Disclaimer.

Correspondence: Uwe B. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. This article has been cited by other articles in PMC. Abstract Monomolecular arrays of protein or glycoprotein subunits forming surface layers S-layers are one of the most commonly observed prokaryotic cell envelope components.

Keywords: crystalline cell surface layers S-layers , bacterial surface layers, self-assembly, nanobiotechnology, biomimetics, synthetic biology. Introduction With the exception of those prokaryotic organisms which have developed strategies to live under very specialized and frequently extreme environmental conditions in which monocultures are feasible, most organisms have to survive in highly competitive habitats in very complex microbiomes.

Table 1 Selected milestones in basic and applied S-layer research. Year Milestone Reference First evidence of a monomolecular array in a bacterial cell wall fragment Houwink Evidence that coherent monomolecular arrays are located on the surface of the cell envelope of intact Gram-positive and Gram-negative bacteria using freeze-etching techniques Remsen et al. Open in a separate window. Figure 1. Occurrence, location, and structure The location and ultrastructure of S-layers of a great number of Bacteria and Archaea have been studied by electron microscopy of thin-sectioned, freeze-etched, freeze-dried and shadowed, negatively stained or frozen hydrated preparations Thornley et al.

Figure 2. Figure 3. Isolation and chemistry In both Archaea and Bacteria , S-layer lattices differ considerably in their susceptibility to isolation from the supporting envelope structure and disruption into monomeric subunits. Assembly and morphogenesis Assembly in vivo Numerous in vitro and in vivo studies have been performed to elucidate the dynamic process of the incorporation and reassembly of new subunits into closed S-layer lattices during cell growth.

Assembly in vitro The capability of isolated S-layer proteins to assemble into two-dimensional arrays in vivo and in vitro is one of their key properties exploited in basic and application-oriented research. Figure 4. Reassembly in solution Self-assembly products are formed in solution during the dialysis of the disrupting agent against selected buffer solutions ionic strength and pH.

Reassembly at interfaces Crystal growth at interfaces e. Genetics, domains, and biosynthesis In the mid-eighties, first reports on cloning and sequencing of S-layer genes were published. Table 2 Functional recombinant S-layer fusion proteins and their applications modified after; Sleytr et al. Tschiggerl pers. Figure 5. Functional aspects When other cell surface components e. S-Layers related to pathogenicity S-layers can contribute to virulence when they are present as a structural component of the cell envelope of pathogens.

S-Layers as adhesion zone for exoenzymes The bacterial cell wall plays a key role in the exchange of substrates between the bacterium and its surrounding environment. S-Layers as template for fine-grain mineralization and bioremediation S-layers are a very common surface structure in Bacteria including Cyanobacteria Smarda et al. S-Layers as matrix for functional molecules and nanoparticles Because S-layer lattices are composed of identical protein or glycoprotein species, functional sequences introduced either by chemical modification or genetic engineering must be aligned in exact positions and orientation down to the subnanometer scale Sleytr et al.

S-layer supported functional lipid membranes The building principle of S-layer supported lipid membranes SsLMs is copied from the supramolecular cell envelope structure of Archaea Fig. Figure 6. S-layer protein—lipid interaction Formation of S-layer lattices covering the entire area of lipid films has been observed on zwitterionic phospholipids such as phosphatidyl cholines and in particular phosphatidyl ethanolamines, but not on negatively charged phospholipids Fig.

Table 3 Summary of membrane-active peptides and transmembrane proteins reconstituted in S-layer supported lipid membranes. S-layer coated liposomes and emulsomes Unilamellar liposomes are artificially prepared spherical containers comprising of a phospholipid bilayer shell and an aqueous core Bangham et al.

Conclusions and perspectives Regular arrays of macromolecules were first observed about 60 years ago in electron micrographs of prokaryotic cell wall fragments and were viewed originally as a curiosity. Acknowledgments The total number of relevant publications currently more than on S-layers far surpasses the number of references that can be cited in this review. Haloferax volcanii archaeosortase is required for motility, mating, and C-terminal processing of the S-layer glycoprotein.

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