Archaeal Cell Walls

Abstract

Next to the bacterial and eukaryal domains, Archaea form the third domain of life. One major difference to bacteria is the composition of the cell wall. The cell wall of most Archaea is formed by a proteinaceous surface (S‐) layer. S‐layer proteins have the intrinsic ability to form two‐dimensional crystals, which can have an oblique (p2), square (p4) or hexagonal (p3 or p6) symmetry. All currently studied archaeal S‐layer proteins were found to be modified by the attachment of N‐linked and, in some cases, additionally by O‐linked glycans. Next to the S‐layer (glyco‐)proteins, sugar polymers like pseudomurein, methanochondroitin or heteropolysaccharides are also found in archaeal cell walls. These polymeric cell wall structures can either form the sole cell wall structure or be supported by an additional S‐layer cover. A few archaeal species even completely lack a cell wall.

Key Concepts:

  • Archaeal cell envelopes lack murein or a lipopolysaccharide (LPS)‐containing outer membrane.

  • Most Archaea posses a glycosylated proteinaceous surface layer (S‐layer) as their sole cell wall structure.

  • In some Archaea, the cell wall is composed of glycan polymers, like glutaminylglycan, heterosaccharide, methanochondroitin or pseudomurein.

Keywords: archaea; cell envelope; glutaminylglycan; glycosylation; heteropolysaccharide; methanochondroitin; pseudomurein; S‐layer (glyco‐)protein

Figure 1.

Diversity of archaeal cell envelopes. Abbreviations: CM, cytoplasmic membrane; GC, glycocalyx; HP, heteropolysaccharide sacculus; MC, methanochondroitin matrix; OM, outermost membrane; PM, pseudomurein; PS, proteinaceous sheath; SL, S‐layer.

Figure 2.

The different S‐layer symmetries. Single S‐layer proteins are depicted. S‐layer proteins that form the respective symmetry units are depicted in red.

Figure 3.

Schematic depiction of the archaeal glycosylation pathways. The N‐glycan biosynthesis starts at the cytoplasmic side of the membrane where nucleotide‐activated monosaccharide sugar precursors are sequentially added onto the lipid carrier dolichyl phosphate or dolichyl pyrophosphate by specific glycosyltransferases (yellow). In the later assembly steps, DolP‐linked monosaccharide might also be used as the sugar donor. The fully assembled DolP(P)‐linked N‐glycan is translocated across the cytoplasmic membrane by an unknown flippase (green) and the oligosaccharide is transferred by the oligosaccharyltransferase AglB (blue) onto a secreted target protein (S‐layer, brown) onto specific aspartic acid residues within N‐glycosylation sequins (Asp‐X‐Ser/Thr). Before protein secretion, specific O‐glycosyltransferases sequentially transfer nucleotide‐activated sugar precursors onto the hydroxyl group of Ser or Thr residues.

Figure 4.

Chemical structure of pseudomurein. After Kandler and König ().

Figure 5.

Putative biosynthetic pathway of pseudomurein according to König et al. (). Stage I – Cytoplasmic stage: formation of the UDP‐activated disaccharide and the UDP‐activated pentapeptide intermediates. Stage II – Cytoplasmic stage: formation of the UDP‐activated disaccharide pentapeptide. Stage III – Lipid stage: formation of undecaprenyl pyrophosphate (UdP‐PP) pentapeptide and tetrapeptide intermediates. During transpeptidation, one C‐terminal alanine residue is split off.

Figure 6.

Proposed structure of the repeating units (regions 1–3) of the cell wall polymer of Natronococcus occultus. Based on Niemetz et al. ().

Figure 7.

Chemical structure of methanochondroitin. After Kreisl and Kandler ().

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References

Albers SV and Meyer BH (2011) The archaeal cell envelope. Nature Reviews Microbiology 9(6): 414–426.

Beveridge TJ and Graham LL (1991) Surface‐layers of bacteria. Microbiological Reviews 55(4): 684–705.

Beveridge TJ, Patel GB, Harris BJ and Sprott GD (1986) The ultrastructure of Methanothrix concilii, a mesophilic aceticlastic Methanogen. Canadian Journal of Microbiology 32(9): 703–710.

Beveridge TJ, Stewart M, Doyle RJ and Sprott GD (1985) Unusual stability of the Methanospirillum hungatei sheath. Journal of Bacteriology 162(2): 728–737.

Biavati B, Vasta M and Ferry JG (1988) Isolation and characterization of Methanosphaera cuniculi sp. nov. Applied and Environmental Microbiology 54(3): 768–771.

Bolhuis H, Palm P, Wende A et al. (2006) The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genomics 7: 169.

Burghardt T, Nather DJ, Junglas B, Huber H and Rachel R (2007) The dominating outer membrane protein of the hyperthermophilic archaeum Ignicoccus hospitalis: a novel pore‐forming complex. Molecular Microbiology 63(1): 166–176.

Burns DG, Janssen PH, Itoh T et al. (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. International Journal of Systematic and Evolutionary Microbiology 57(Pt 2): 387–392.

Chung S, Shin SH, Bertozzi CR and De Yoreo JJ (2010) Self‐catalyzed growth of S layers via an amorphous‐to‐crystalline transition limited by folding kinetics. Proceedings of the National Academy of Sciences of the USA 107(38): 16536–16541.

Eichler J (2013) Extreme sweetness: protein glycosylation in archaea. Nature Reviews Microbiology 11(3): 151–156.

Firtel M, Patel GB and Beveridge TJ (1995) S‐layer regeneration in Methanococcus voltae protoplasts. Microbiology 141: 817–824.

Firtel M, Southam G, Harauz G and Beveridge TJ (1993) Characterization of the cell wall of the sheathed methanogen Methanospirillum hungatei Gp1 as an S‐Layer. Journal of Bacteriology 175(23): 7550–7560.

Formanek H (1985) 3‐dimensional models of the carbohydrate moieties of murein and pseudomurein. Zeitschrift für Naturforschung C 40(7–8): 555–561.

Hartmann E and König H (1991) Nucleotide‐activated oligosaccharides are intermediates of the cell wall polysaccharide of Methanosarcina barkeri. Biological Chemistry Hoppe‐Seyler 372(11): 971–974.

Houwink AL and Le Poole JB (1952) Eine Struktur in der Zellmembran einer Bakterie. Physikalische Verhandlungen 3(98) .

Johannsen L, Labischinski H and Krueger JM (1991) Somnogenic activity of pseudomurein in rabbits. Infection and Immunity 59(7): 2502–2504.

Kandler O and König H (1978) Chemical composition of peptidoglycan free cell‐walls of methanogenic bacteria. Archives of Microbiology 118(2): 141–152.

Kandler O and König H (1985) Cell envelopes of Archaebacteria. In: Woese C and Wolfe R (eds) The Bacteria. A Treatise on Structure and Function, vol. VIII, pp. 413–457. New York: Academic Press.

Kandler O and König H (1993) Cell envelopes of archaea: structure and chemistry. In: Kates M, Kusher D and Matheson AT (eds) The Biochemistry of Archaea, pp. 223–259. Amsterdam: Elsevier.

Kiener A, König H, Winter J et al. (1987) Purification and use of Methanobacterium wolfei psuedomurein endopeptidase for lysis of Methanobacterium thermoautotrophicum. Journal of Bacteriology 169(3): 1010–1016.

Kocur M, Martinec T and Smid B (1972) Fine structure of extreme halophilic cocci. Microbios 5(18): 101–107.

König H (1986) Chemical composition of cell envelopes of methanogenic bacteria isolated from human and animal feces. Systematic and Applied Microbiology 8(3): 159–162.

König H (1988) Archaeobacterial cell envelopes. Canadian Journal of Microbiology 34(4): 395–406.

König H, Hartmann E and Karcher U (1994) Pathways and principles of the biosynthesis of methanobacterial cell‐wall polymers. Systematic and Applied Microbiology 16(4): 510–517.

König H, Kralik R and Kandler O (1982) Structure and modifications of pseudomurein in Methanobacteriales. Zentralblatt fur Bakteriologie Mikrobiologie und Hygiene I Abteilung Originale C 33(2): 179–191.

Kreisl P and Kandler O (1986) Chemical structure of the cell‐wall polymer of Methanosarcina. Systematic and Applied Microbiology 7(2–3): 293–299.

Küper U, Meyer C, Müller V, Rachel R and Huber H (2010) Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis. Proceedings of the National Academy of Sciences of the USA 107(7): 3152–3156.

Kurr M, Huber R, König H et al. (1991) Methanopyrus kandleri, gen. and sp. nov represents a novel group of hyperthermophilic methanogens, growing at 110 degrees C. Archives of Microbiology 156(4): 239–247.

Labischinski H, Barnickel G, Leps B, Bradaczek H and Giesbrecht P (1980) Initial data for the comparison of murein and pseudomurein conformations. Archives of Microbiology 127(3): 195–201.

Lechner J and Wieland F (1989) Structure and biosynthesis of prokaryotic glycoproteins. Annual Review of Biochemistry 58: 173–194.

Leps B, Labischinski H, Barnickel G, Bradaczek H and Giesbrecht P (1984) A new proposal for the primary and secondary structure of the glycan moiety of pseudomurein ‐ conformational energy calculations on the glycan strands with talosaminuronic acid in 1c conformation and comparison with murein. European Journal of Biochemistry 144(2): 279–286.

Mescher MF, Hansen U and Strominger JL (1976) Formation of lipid‐linked sugar compounds in Halobacterium salinarium. Presumed intermediates in glycoprotein synthesis. Journal of Biological Chemistry 251(23): 7289–7294.

Mescher MF and Strominger JL (1976) Purification and characterization of a prokaryotic glycoprotein from cell envelope of Halobacterium salinarium. Journal of Biological Chemistry 251(7): 2005–2014.

Meyer BH and Albers SV (2013) Hot and sweet: protein glycosylation in Crenarchaeota. Biochemical Society Transactions 41(1): 384–392.

Niemetz R, Karcher U, Kandler O, Tindall BJ and König H (1997) The cell wall polymer of the extremely halophilic archaeon Natronococcus occultus. European Journal of Biochemistry 249(3): 905–911.

Patel GB, Sprott GD, Humphrey RW and Beveridge TJ (1986) Comparative analyses of the sheath structures of Methanothrix‐concilii Gp6 and Methanospirillum‐hungatei strains Gp1 and Jf1. Canadian Journal of Microbiology 32(8): 623–631.

Pum D, Messner P and Sleytr UB (1991) Role of the S‐layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense. Journal of Bacteriology 173(21): 6865–6873.

Robinson RW, Aldrich HC, Hurst SF and Bleiweis AS (1985) Role of the cell‐surface of Methanosarcina mazei in cell aggregation. Applied and Environmental Microbiology 49(2): 321–327.

Schleifer KH, Steber J and Mayer H (1982) Chemical composition and structure of the cell wall of Halococcus morrhuae. Zentralblatt fur Bakteriologie Mikrobiologie und Hygiene I Abteilung Originale C C3: 171–178.

Sheehan JK, Thornton DJ, Somerville M and Carlstedt I (1991) The structure and heterogeneity of respiratory mucus glycoproteins. American Review of Respiratory Disease 144(3): S4–S9.

Sprott GD, Colvin JR and Mckellar RC (1979) Spheroplasts of Methanospirillum hungatii formed upon treatment with dithiothreitol. Canadian Journal of Microbiology 25(6): 730–738.

Sprott GD and Mckellar RC (1980) Composition and properties of the cell wall of Methanospirillum hungatii. Canadian Journal of Microbiology 26(2): 115–120.

Steber J and Schleifer KH (1975) Halococcus morrhuae – Sulfated heteropolysaccharide as structural component of bacterial cell wall. Archives of Microbiology 105(2): 173–177.

Sumper M, Berg E, Mengele R and Strobel I (1990) Primary structure and glycosylation of the S‐layer protein of Haloferax volcanii. Journal of Bacteriology 172(12): 7111–7118.

Vinogradov E, Deschatelets L, Lamoureux M et al. (2012) Cell surface glycoproteins from Thermoplasma acidophilum are modified with an N‐linked glycan containing 6‐C‐sulfofucose. Glycobiology 22(9): 1256–1267.

Wirth R, Bellack A, Bertl M et al. (2011) The mode of cell wall growth in selected Archaea is similar to the general mode of cell wall growth in bacteria as revealed by fluorescent dye analysis. Applied and Environmental Microbiology 77(5): 1556–1562.

Woese CR and Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences of the USA 74(11): 5088–5090.

Yang LL and Haug A (1979) Purification and partial characterization of a procaryotic glycoprotein from the plasma‐membrane of Thermoplasma acidophilum. Biochimica Et Biophysica Acta 556(2): 265–277.

Zeikus JG and Bowen VG (1975) Fine‐structure of Methanospirillum hungatii. Journal of Bacteriology 121(1): 373–380.

Further Readings

Baumeister W and Lembcke G (1992) Structural features of archaebacterial cell envelopes. Journal of Bioenergetics and Biomembranes 24(6): 567–575.

Claus H and König H (2010) Cell envelopes of methanogens. In: Claus H and König H (eds) Prokaryotic Cell Wall Compounds, chap. 7, pp. 231–252. Heidelberg: Springer.

Eichler J, Abu‐Qarn M, Konrad Z et al. (2010) The cell envelopes of haloarchaea: staying in shape in a world of salt. In: Claus H and König H (eds) Prokaryotic Cell Wall Compounds, chap. 8, pp. 253–270. Heidelberg: Springer.

Eichler J and Adams MW (2005) Posttranslational protein modification in Archaea. Microbiology and Molecular Biology Reviews 69(3): 393–425.

König H (1988) Archaeobacterial cell envelopes. Canadian Journal of Microbiology 34(4): 395–406.

Rachel R (2010) Cell envelopes of crenarchaeota and nanoarchaeota. In: Claus H and König H (eds) Prokaryotic Cell Wall Compounds, chap. 9, pp. 271–291. Heidelberg: Springer.

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Meyer, Benjamin H, and Albers, Sonja‐Verena(Feb 2014) Archaeal Cell Walls. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000384.pub2]