Archaeal Cell Walls

Abstract

Next to the bacterial and eukaryal domains, Archaea form one of the three domains of life. Within the last decade, the phylogenetic tree of archaea has dramatically expanded and nowadays Archaea are found in almost every habitat, from extreme to moderate. The adaptation to these diverse environments might have resulted in the remarkably high variety of different archaeal cell envelope types. One major difference to bacteria is the lack of murein or a lipopolysaccharide (LPS)‐containing outer membrane.

The cell wall of many 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. However, also Archaea have been characterised which lack an S‐layer and possess instead a second outermost membrane or sugar polymers like pseudomurein, methanochondroitin, or heteropolysaccharides as their cell envelope. These polymeric cell wall structures can either form the sole cell wall structure or be supported by an additional S‐layer cover.

Key Concepts

  • Archaea do have peptidoglycan, it is called pseudomurein and different in its composition to murein.
  • Most studied Archaea have one cytoplasmic membrane, but more and more species are found which have two membranes.
  • Archaeal cell envelopes lack murein or a lipopolysaccharide (LPS)‐containing outer membrane.
  • Many Archaea possess 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, which can be further supported by an S‐layer.

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 N‐ and O‐glycosylation pathways in the crenarchaeaon S. acidocaldarius (a) and the model of the pseudomurein biosynthesis pathway (b). (a) The N‐glycan biosynthesis starts at the cytoplasmic side of the membrane where nucleotide‐ or lipid‐phosphate‐ activated monosaccharide sugar precursors (e.g. UDP‐GlcNAc, or dolichol‐phosphate‐mannose) are sequentially added onto the lipid carrier dolichol phosphate (Euryarchaeota) or dolichol pyrophosphate (Crenarchaeota) by multiple specific glycosyltransferases (yellow). The fully assembled DolP(P)‐linked N‐glycan is translocated across the cytoplasmic membrane by an unknown flippase and the oligosaccharide is transferred by the oligosaccharyltransferase AglB (blue) onto a secreted target protein (Sec secretion system, green; S‐layer, brown) onto specific aspartic acid residues within N‐glycosylation sequins (Asp‐X‐Ser/Thr). So far no biosynthesis study on the O‐glycosylation process in Archaea has been performed. It is proposed that before protein secretion, specific O‐glycosyltransferases sequentially transfer nucleotide‐activated sugar precursors onto the hydroxyl group of Ser or Thr residues on to the target protein. (b) Putative biosynthetic pathway of pseudomurein. Based on homologs of the bacterial MraY and MurG in pseudomurein synthesising archaea, a new pathway has been here predicted. Similar to the bacterial peptidoglycan the biosynthesis starts with the formation of N‐acetyl‐l‐talosaminuronic acid (TalNAcA), which is then attached with Glc, Ala, and Lys residues. This TalNAcA pentapeptide and tetrapeptide is transferred onto a lipid carrier, by a MraY homolog enzyme and further enlarged by the attachment of N‐acetyl‐d‐glucosamine or N‐acetyl‐d‐galactosamine via a β‐1,3 linkage. Flipped across the membrane and assembled by transglycosyadases and transpeptidases into the pseudomurein polymer. During transpeptidation, one C‐terminal alanine residue is predicted to split off.
Figure 4. Chemical structure of pseudomurein. Adapted from Kandler and König .
Figure 5. Proposed structure of the repeating units (regions 1–3) of the cell wall polymer of Natronococcus occultus. Based on Niemetz et al. .
Figure 6. Chemical structure of methanochondroitin. From Kreisl and Kandler .
close

References

Abdul‐Halim MF, Schulze S, DiLucido A, et al. (2019) Lipid anchoring of the archaeosortase substrates and mid‐cell grwoth in Haloarchaea. bioRxiv: 863746.

Ajon M, Frols S, van Wolferen M, et al. (2011) UV‐inducible DNA exchange in hyperthermophilic Archaea mediated by type IV pili. Molecular Microbiology 82 (4): 807–817.

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

Albers S, Eichler J and Aebi M (2017) Archaea. In: Varki A, Cummings RD, Esko JD, et al. (eds) Essentials of Glycobiology, 3rd edn, pp 283–292. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.

Atomi H, Fukui T, Kanai T, et al. (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1 (4): 263–267.

Baker BJ, Tyson GW, Webb RI, et al. (2006) Lineages of acidophilic archaea revealed by community genomic analysis. Science 314 (5807): 1933–1935.

Baker BJ, Comolli LR, Dick GJ, et al. (2010) Enigmatic, ultrasmall, uncultivated Archaea. Proceedings of the National Academy of Sciences of the United States of America 107 (19): 8806–8811.

Baumeister W, Santarius U, Volker S, et al. (1990) The Surface protein of Hyperthermus butylicus ‐ 3‐dimensional structure and comparison with other archaebacterial surface‐proteins. Systematic and Applied Microbiology 13 (2): 105–111.

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

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

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.

Brochier C, Forterre P and Gribaldo S (2005) An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evolutionary Biology 5: 36.

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

Burghardt T, Saller M, Gurster S, et al. (2008) Insight into the proteome of the hyperthermophilic crenarchaeon Ignicoccus hospitalis: the major cytosolic and membrane proteins. Archives of Microbiology 190 (3): 379–394.

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.

Chaban B, Ng SY and Jarrell KF (2006) Archaeal habitats‐from the extreme to the ordinary. Canadian Journal of Microbiology 52 (2): 73–116.

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 United States of America 107 (38): 16536–16541.

Comolli LR, Baker BJ, Downing KH, et al. (2009) Three‐dimensional analysis of the structure and ecology of a novel, ultra‐small archaeon. The ISME Journal 3 (2): 159–167.

DeLong EF and Pace NR (2001) Environmental diversity of Bacteria and Archaea. Systematic Biology 50 (4): 470–478.

Dridi B, Fardeau ML, Ollivier B, et al. (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology 62 (Pt 8): 1902–1907.

Eichler J (2020) Modifying post‐translational modifications: A strategy used by Archaea for adapting to changing environments?: Manipulating the extent, position, or content of post‐translational modifications may help Archaea adapt to environmental change. Bioessays 42 (3): e1900207.

Eme L, Spang A, Lombard J, et al. (2017) Archaea and the origin of eukaryotes. Nature Reviews Microbiology 15 (12): 711–723.

Erauso G, Reysenbach A‐L, Godfroy A, et al. (1993) Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep‐sea hydrothermal vent. Archives of Microbiology 160 (5): 338–349.

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.

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

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

Gambelli L, Meyer BH, McLaren M, et al. (2019) Architecture and modular assembly of Sulfolobus S‐layers revealed by electron cryotomography. Proceedings of the National Academy of Sciences of the United States of America 116 (50): 25278–25286.

Godfroy A, Meunier JR, Guezennec J, et al. (1996) Thermococcus fumicolans sp. nov., a new hyperthermophilic archaeon isolated from a deep‐sea hydrothermal vent in the north Fiji Basin. International Journal of Systematic and Evolutionary Microbiology 46 (4): 1113–1119.

Gongadze GM, Kostyukova AS, Miroshnichenko ML and Bonch‐Osmolovskaya EA (1993) Regular proteinaceous layers of Thermococcus stetteri cell envelope. Current Microbiology 27 (1): 5–9.

Gorlas A, Croce O, Oberto J, et al. (2014) Thermococcus nautili sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal deep‐sea vent. International Journal of Systematic and Evolutionary Microbiology 64 (Pt 5): 1802–1810.

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.

Heimerl T, Flechsler J, Pickl C, et al. (2017) A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Frontiers in Microbiology 8: 1072.

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

Huber R, Stohr J, Hohenhaus S, et al. (1995) Thermococcus Chitonophagus sp. nov, a novel, chitin‐degrading, hyperthermophillic archaeum from a deep‐sea hydrothermal vent environment. Archives of Microbiology 164 (4): 255–264.

Jahn U, Summons R, Sturt H, et al. (2004) Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Archives of Microbiology 182 (5): 404–413.

Jarrell KF, Ding Y, Meyer BH, et al. (2014) N‐linked glycosylation in Archaea: a structural, functional, and genetic analysis. Microbiology and Molecular Biology Reviews 78 (2): 304–341.

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. Academic Press: New York.

Kandler O and König H (1993) Chapter 8 cell envelopes of archaea: structure and chemistry. In: Kates M, Kushner D and Matheson A (eds) New Comprehensive Biochemistry, vol. 26, pp 223–259. Elsevier: New York.

Kandler O and König H (1998) Cell wall polymers in Archaea (Archaebacteria). Cellular and Molecular Life Sciences 54 (4): 305–308.

Kiener A, König H, Winter J and Leisinger T (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, Kralik R and Kandler O (1982) Structure and modifications of pseudomurein in Methano‐bacleriales. Zentralblatt für Bakteriologie Mikrobiologie und Hygiene: I. Abt. Originale C: Allgemeine, angewandte und ökologische Mikrobiologie 3 (2): 179–191.

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

Koskinen K, Pausan MR, Perras AK, et al. (2017) First Insights into the diverse human archaeome: specific detection of Archaea in the gastrointestinal tract, lung, and nose and on skin. MBio 8 (6): e00824‐17.

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, et al. (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 United States of America 107 (7): 3152–3156.

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

Leps B, Labischinski H, Barnickel G, et al. (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 and Strominger JL (1976a) Purification and characterization of a prokaryotic glycoprotein from cell envelope of Halobacterium salinarium. Journal of Biological Chemistry 251 (7): 2005–2014.

Mescher MF and Strominger JL (1976b) Structural (shape maintaining) role of cell surface glycoprotein of Halobacterium salinarium. Proceedings of the National Academy of Sciences of the United States of America 73 (8): 2687–2691.

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

Miroshnichenko ML, Bonch‐Osmolovskaya EA, Neuner A, et al. (1989) Thermococcus stetteri sp. nov., a new extremely thermophilic marine sulfur‐metabolizing archaebacterium. Systematic and Applied Microbiology 12 (3): 257–262.

Moissl C, Rudolph C, Rachel R, et al. (2003) In situ growth of the novel SM1 euryarchaeon from a string‐of‐pearls‐like microbial community in its cold biotope, its physical separation and insights into its structure and physiology. Archives of Microbiology 180 (3): 211–217.

Niemetz R, Kärcher U, Kandler O, et al. (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.

Paul K, Nonoh JO, Mikulski L and Brune A (2012) “Methanoplasmatales,” Thermoplasmatales‐related archaea in termite guts and other environments, are the seventh order of methanogens. Applied and Environmental Microbiology 78 (23): 8245–8253.

Perras AK, Wanner G, Klingl A, et al. (2014) Grappling archaea: ultrastructural analyses of an uncultivated, cold‐loving archaeon, and its biofilm. Frontiers in Microbiology 5: 397.

Phipps BM, Huber R and Baumeister W (1991) The cell envelope of the hyperthermophilic archaebacterium Pyrobaculum organotrophum consists of two regularly arrayed protein layers – three‐dimensional structure of the outer layer. Molecular Microbiology 5 (2): 253–265.

Probst AJ, Weinmaier T, Raymann K, et al. (2014) Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nature Communications 5: 5497.

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.

Rachel R, Wyschkony I, Riehl S and Huber H (2002) The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1 (1): 9–18.

Rachel R (2010) Cell Envelopes of Crenarchaeota and Nanoarchaeota. Springer: Heidelberg.

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 für Bakteriologie Mikrobiologie und Hygiene: I. Abt. Originale C: Allgemeine, angewandte und ökologische Mikrobiologie 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.

Taguchi Y, Fujinami D and Kohda D (2016) Comparative analysis of archaeal lipid‐linked oligosaccharides that serve as oligosaccharide donors for Asn glycosylation. Journal of Biological Chemistry 291 (21): 11042–11054.

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 United States of America 74 (11): 5088–5090.

van Wolferen M, Shajahan A, Heinrich K, et al. (2019) Species‐specific recognition of Sulfolobales mediated by UV‐inducible pili and S‐layer glycosylation patterns. bioRxiv: 663898.

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.

Zhang C, Wipfler RL, Li Y, et al. (2019) Cell structure changes in the hyperthermophilic crenarchaeon Sulfolobus islandicus lacking the S‐Layer. mBio 10 (4): e01589‐19.

Zillig W, Holz I, Klenk H‐P, et al. (1987) Pyrococcus woesei, sp. nov., an ultra‐thermophilic marine archaebacterium, representing a novel order, Thermococcales. Systematic and Applied Microbiology 9 (1): 62–70.

Zink IA, Pfeifer K, Wimmer E, et al. (2019) CRISPR‐mediated gene silencing reveals involvement of the archaeal S‐layer in cell division and virus infection. Nature Communications 10 (1): 4797.

Further Reading

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, chapter 7, pp 231–252. Springer: Heidelberg.

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

Jarrell KF, Ding Y, Meyer BH, et al. (2014) N‐linked glycosylation in Archaea: a structural, functional, and genetic analysis. Microbiology and Molecular Biology Reviews 78 (2): 304–341.

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, chapter 9, pp 271–291. Springer: Heidelberg.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Meyer, Benjamin H, and Albers, Sonja‐Verena(Jul 2020) Archaeal Cell Walls. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000384.pub3]