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Protein secretion in the Archaea: multiple paths towards a unique cell surface

Nature Reviews Microbiology volume 4, pages 537–547 (2006)Cite this article

Key Points

  • Archaea represent the third domain of life. Many of these prokaryotes thrive under extreme environmental conditions. The structure of their cell envelope differs substantially from that of other prokaryotes, which is related to their eccentric way of life, but also to the distinct solutions required to assemble their unique cellular surface.

  • The Sec (secretion) pathway is the only protein-translocation pathway in nature known to be universally conserved. The Sec translocase mediates the translocation of unfolded proteins across, and the insertion of membrane proteins into, the membrane. The archaeal Sec translocase seems to be mosaic with features that are similar to the Sec translocase of bacteria or eukaryotic endoplasmic reticulum.

  • The Tat (twin arginine translocation) translocase allows the transmembrane translocation of proteins in their fully folded state. This pathway is present in most prokaryotes, and chloroplasts, but it is not essential for viability. Some halophilic archaea depend on the Tat system for viability, and most secretory proteins seem to use this pathway for secretion, indicating a specific adaptation to high saline environments.

  • Most archaea are covered by a surface layer (S-layer) that consists of a crystalline layer of glycoproteins with pores that are permeable to solute and small proteins. Several types of appendage extend from the archaeal cell surface, such as pili and flagella, and also novel structures that are needed for surface attachment and efficient nutrient acquisition in their natural habitat. The assembly of these structures involves transport systems with subunits that are homologous to the cytoplasmic membrane components of bacterial type II and IV secretion systems, but that seem less complex.

Abstract

Archaea are similar to other prokaryotes in most aspects of cell structure but are unique with respect to the lipid composition of the cytoplasmic membrane and the structure of the cell surface. Membranes of archaea are composed of glycerol-ether lipids instead of glycerol-ester lipids and are based on isoprenoid side chains, whereas the cell walls are formed by surface-layer proteins. The unique cell surface of archaea requires distinct solutions to the problem of how proteins cross this barrier to be either secreted into the medium or assembled as appendages at the cell surface.

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Figure 1: Cell envelope of archaea.
Figure 2: Mosaic subunit composition of the Sec translocase in archaea.
Figure 3: Schematic representation of the conserved signal-recognition particle pathway.
Figure 4: Membrane topology of the Haloferax volcanii Tat translocase subunits.
Figure 5: Model of the assembly of cell appendices in the cell envelope of Sulfolobus solfataricus.

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Acknowledgements

This work was supported by a van der Leeuw grant to A.J.M.D. from the Earth and Life Sciences Foundation (ALW) which is subsidized by the Dutch Organization for Scientific Research (NWO), and Veni and Vidi grants to S.-V.A. from NWO.

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Author notes

  1. Sonja-Verena Albers and Zalán Szabó: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute and the Materials Science Centre Plus, University of Groningen, Kerklaan 30, HAREN, 9751 NN, The Netherlands

    Sonja-Verena Albers, Zalán Szabó & Arnold J. M. Driessen

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  1. Sonja-Verena Albers
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  2. Zalán Szabó
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  3. Arnold J. M. Driessen
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Correspondence to Arnold J. M. Driessen.

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DATABASES

Entrez Genome Project

Archaeoglobus fulgidus

Escherichia coli

Haloarcula marismortui

Halobacterium salinarum NRC-1

Haloferax volcanii

Methanocaldococcus jannaschii

Methanococcus maripaludis

Methanococcus voltae

Natronomonas pharaonis

Picrophilus torridus

Pseudomonas aeruginosa

Saccharomyces cerevisiae

Salinibacter ruber

Sulfolobus acidocaldarius

Sulfolobus solfataricus

Vibrio cholerae

FURTHER INFORMATION

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Glossary

Halophile

A microorganism that requires high levels of sodium chloride, usually above 0.2 M, to grow. Extreme halophiles, most of which are archaea, inhabit water that is up to 10 times more saline than seawater.

Hyperthermophile

A microorganism that has an optimal growth temperature between 80°C and approximately 113°C. Some hyperthermophiles are found in geysers and black smokers.

Isoprenyl groups

Building blocks of the acyl chain of archaeal lipids, representing repeating units of the five-carbon hydrocarbon isoprene, the common synonym for the chemical compound 2-methyl-1,3-butadiene.

Mesophile

A microorganism that grows optimally at temperatures between 20?45°C. Some archaea are mesophiles and are found in environments such as marshland, sewage and soil, whereas many methogenic archaea live in the digestive tracts of humans, and animals such as ruminants and termites.

Chloroplast thylakoid membrane

Chloroplasts are organelles found in plant cells and eukaryotic algae that conduct photosynthesis. They are generally considered to have originated as endosymbiotic cyanobacteria.Thylakoids are membrane-bound compartments, internal to chloroplasts. The thylakoid membrane contains integral membrane-protein complexes that capture light energy from the sun to produce the free energy stored in ATP and NADPH.

F1F0-ATP synthase

An enzyme that can synthesize adenosine triphosphate (ATP) from adenosine diphosphate (ADP) and inorganic phosphate by using the transmembrane proton gradient as a source of energy. The F1 portion of the ATP synthase is above the bacterial cytoplasmic membrane, and constitutes the catalytic domain that contains the nucleotide binding sites. The F0 portion is membrane-integral and conducts the transmembrane movement of protons, which is coupled to the synthesis or hydrolysis of ATP through the F1 portion.

Amphipathic helix

An amphipathic molecule contains both hydrophobic and hydrophilic groups. An amphipathic helix consists of a polypeptide chain with a hydrophobic surface and a hydrophilic surface.

Polytopic membrane protein

A membrane protein containing multiple membrane-spanning helical domains that are embedded in the membrane by hydrophobic interactions with the lipid interior of the bilayer.

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Albers, SV., Szabó, Z. & Driessen, A. Protein secretion in the Archaea: multiple paths towards a unique cell surface. Nat Rev Microbiol 4, 537–547 (2006). https://doi.org/10.1038/nrmicro1440

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