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  • Review Article
  • Published:

Biogenesis and functions of bacterial S-layers

Nature Reviews Microbiology volume 12, pages 211–222 (2014)Cite this article

Subjects

Key Points

  • S-layers are two-dimensional (2D) protein arrays that are frequently found on the surface of bacteria and archaea.

  • Genetic analysis reveals a wide diversity of genes that encode S-layer proteins (SLPs) in some species, and several mechanisms are found to facilitate gene switching and regulation.

  • Secretion of S-layer proteins often involves a dedicated secretion system, such as accessory Sec systems in Bacillus anthracis and Clostridium difficile, and a wide range of mechanisms for anchoring S-layers to the underlying cell envelope have been identified.

  • Gram-positive species, including B. anthracis and C. difficile, possess large families of genes encoding proteins that are related to the S-layer protein and that share a common anchoring mechanism.

  • In many species, the SLPs are glycosylated. Dedicated glycosylation loci are found that specify all the genes that are necessary for the synthesis of glycan, its secretion across the membrane and ligation to the SLP via N- or O- linkages.

  • S-layers have been the subject of intensive structural analysis since their identification in the 1950s. Recent efforts are gradually improving our high-resolution structural knowledge of various S-layer proteins and finally enabling reasonable quality models of an entire S-layer to be made.

  • SLPs have evolved to mediate a broad range of functions, including biogenesis of the cell wall, control of cell division and specialized activities, such as swimming. In pathogens, SLPs can interfere with the immune system and can aid survival via adhesion to host cells. In Gram-positive bacteria, functions are often associated with an effector domain that can confer properties that are distinct from the ability to form a 2D array.

Abstract

The outer surface of many archaea and bacteria is coated with a proteinaceous surface layer (known as an S-layer), which is formed by the self-assembly of monomeric proteins into a regularly spaced, two-dimensional array. Bacteria possess dedicated pathways for the secretion and anchoring of the S-layer to the cell wall, and some Gram-positive species have large S-layer-associated gene families. S-layers have important roles in growth and survival, and their many functions include the maintenance of cell integrity, enzyme display and, in pathogens and commensals, interaction with the host and its immune system. In this Review, we discuss our current knowledge of S-layer and related proteins, including their structures, mechanisms of secretion and anchoring and their diverse functions.

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Figure 1: Clostridium difficile and Bacillus anthracis cell surface protein families.
Figure 2: Secretion of bacterial S-layer proteins.
Figure 3: Functions of S-layer proteins.

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Acknowledgements

Work in the N.F.F. laboratory is currently supported by the MRC (grants G0800170 and G1001721), the Wellcome Trust (grant 090969Z) and the Leverhulme Trust (grant RF2012-232), and work in the R.P.F. laboratory is supported by the University of Sheffield, UK.

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Authors and Affiliations

  1. Department of Molecular Biology and Biotechnology, University of Sheffield, S10 2TN, UK

    Robert P. Fagan

  2. Department of Life Sciences, MRC Centre for Molecular Bacteriology and Infection, Imperial College London, SW7 2AZ, UK

    Neil F. Fairweather

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  1. Robert P. Fagan
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Correspondence to Neil F. Fairweather.

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Supplementary information

Supplementary information S1 (table)

Identification of putative functional domains in the B. anthracis and C. difficile cell surface protein families (PDF 206 kb)

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Glossary

Phase-variable expression

The random variation of gene expression in a bacterial population. Expression in individual cells is either on or off, leading to phenotypic heterogeneity in the population.

Type I secretion system

A sec-independent protein secretion system in Gram-negative bacteria. It consists of an inner membrane ATP-binding cassette (ABC) transporter, a periplasmic membrane fusion protein and an outer membrane pore.

Type II secretion systems

sec-dependent multiprotein secretion systems in Gram-negative bacteria; they are closely related to type IV pili.

Secondary cell wall polymer

(SCWP). A carbohydrate-based polymer, other than peptidoglycan and anionic polymers, that is present in the cell wall — for example, the pyruvylated Bacillus anthracis SCWP that anchors the S-layer proteins EA1 and Sap to the cell wall.

N- and O-linkages

Linkage of a sugar to the nitrogen (N) atom of asparagine or to the oxygen (O) atom of serine, threonine or tyrosine.

Sacculi

The sacs of polymerized peptidoglycan that surround bacteria. When they are isolated from the bacterium, they retain the shape of the cell.

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Fagan, R., Fairweather, N. Biogenesis and functions of bacterial S-layers. Nat Rev Microbiol 12, 211–222 (2014). https://doi.org/10.1038/nrmicro3213

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