Antonie van Leeuwenhoek

, Volume 102, Issue 2, pp 203–219 | Cite as

The unusual cell biology of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis

  • Harald Huber
  • Ulf Küper
  • Stefanie Daxer
  • Reinhard Rachel
Invited Review Paper


The Crenarchaeon Ignicoccus hospitalis is an anaerobic, obligate chemolithoautotrophic hyperthermophile, growing by reduction of elemental sulfur using molecular hydrogen as electron donor. Together with Nanoarchaeum equitans it forms a unique, archaeal biocoenosis, in which I. hospitalis serves as host for N. equitans. Both organisms can be cultivated in a stable coculture which is mandatory for N. equitans but not for I. hospitalis. This strong dependence is affirmed by the fact that N. equitans obtains its lipids and amino acids from the host. I. hospitalis cells exhibit several unique features: they can adhere to surfaces by extracellular appendages (‘fibers’) which are not used for motility; they use a novel CO2 fixation pathway, the dicarboxylate/4-hydroxybutyrate pathway; and they exhibit a unique cell envelope for Archaea consisting of two membranes but lacking an S-layer. These membranes form two cell compartments, a tightly packed cytoplasm surrounded by a weakly staining intermembrane compartment (IMC) with a variable width from 20 to 1,000 nm. In this IMC, many round or elongated vesicles are found which may function as carriers of lipids or proteins out of the cytoplasm. Based on immuno-EM analyses and immuno-fluorescence experiments it was demonstrated recently that the A1AO ATP synthase, the H2:sulfur oxidoreductase complex and the acetyl-CoA synthetase (ACS) of I. hospitalis are located in its outermost membrane. Therefore, this membrane is energized and is here renamed as “outer cellular membrane” (OCM). Among all prokaryotes possessing two membranes in their cell envelope, I. hospitalis is the first organism with an energized outermost membrane and ATP synthesis outside the cytoplasm. Since DNA and ribosomes are localized in the cytoplasm, energy conservation is separated from information processing and protein biosynthesis in I. hospitalis. This raises questions concerning the function and characterization of the two membranes, the two cell compartments and of a possible ATP transfer to N. equitans.


Ignicoccus hospitalis Cell biology Archaea ATP synthase Cell compartimentation Immuno-localization Nanoarchaeum equitans 



We thank Michael Thomm for ongoing support, Reinhard Wirth for stimulating discussions, Carolin Meyer, Thomas Heimerl and Jennifer Flechsler for providing electron micrographs, Ulrike Friedrich for providing data and art work on the carbon metabolism, Thomas Hader and Konrad Eichinger for technical support, and Antje Zenker for art work. This work was supported by Deutsche Forschungsgemeinschaft Grant HU703/2-1 (to H.H. and R.R.).

Supplementary material

10482_2012_9748_MOESM1_ESM.pdf (1005 kb)
Supplementary material 1 (PDF 1,005 kb)


  1. Burghardt T, Näther DJ, Junglas B, Huber H, Rachel R (2007) The dominating outer membrane protein of the hyperthermophilic Archaeum Ignicoccus hospitalis: a novel pore-forming complex. Mol Microbiol 63:166–176PubMedCrossRefGoogle Scholar
  2. Burghardt T, Saller M, Gürster S, Müller D, Meyer C, Jahn U, Hochmuth E, Deutzmann R, Siedler F, Babinger P, Wirth R, Huber H, Rachel R (2008) Insight into the proteome of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis: the major cytosolic and membrane proteins. Arch Microbiol 190:379–394PubMedCrossRefGoogle Scholar
  3. Burghardt T, Junglas B, Siedler F, Wirth R, Huber H, Rachel R (2009) The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells. Biochem Soc Trans 37:127–132PubMedCrossRefGoogle Scholar
  4. Daxer S (2011) Lokalisation stoffwechselrelevanter Enzymkomplexe sowie Anreicherung einer membrangebundenen Pyrophosphatase in Vertretern der archaeellen Gattung Ignicoccus. University of Regensburg, Master thesisGoogle Scholar
  5. Giannone RJ, Huber H, Karpinets T, Heimerl T, Küper U, Rachel R, Keller M, Hettich RL, Podar M (2011) Proteomic characterization of cellular and molecular processes that enable the Nanoarchaeum equitans-Ignicoccus hospitalis relationship. PLoS ONE 6:e22942. doi: 10.1371/journal.pone.0022942 PubMedCrossRefGoogle Scholar
  6. Haferkamp I, Schmitz-Esser S, Wagner M, Neigel N, Horn M, Neuhaus HE (2006) Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol Microbiol 60:1534–1545PubMedCrossRefGoogle Scholar
  7. Hollenstein K, Frei DC, Locher KP (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446:213–216PubMedCrossRefGoogle Scholar
  8. Huber H, Stetter KO (2006) Desulfurococcales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH,. Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York, pp 52–68.
  9. Huber H, Burggraf S, Mayer T, Wyschkony I, Rachel R, Stetter KO (2000) Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov. Int J Syst Evol Microbiol 50:2093–2100PubMedCrossRefGoogle Scholar
  10. Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417:63–67PubMedCrossRefGoogle Scholar
  11. Huber H, Gallenberger M, Jahn U, Eylert E, Berg IA, Kockelkorn D, Eisenreich W, Fuchs G (2008) A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc Natl Acad Sci USA 105:7851–7856PubMedCrossRefGoogle Scholar
  12. Hügler M, Huber H, Stetter KO, Fuchs G (2003) Autotrophic CO2 fixation pathways in Archaea (Crenarchaeota). Arch Microbiol 179:160–173PubMedGoogle Scholar
  13. Jahn U, Summons R, Sturt H, Grosjean E, Huber H (2004) Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Arch Microbiol 182:404–413PubMedCrossRefGoogle Scholar
  14. Jahn U, Huber H, Eisenreich W, Hügler M, Fuchs G (2007) Insights into the autotrophic CO2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism. J Bacteriol 189:4108–4119PubMedCrossRefGoogle Scholar
  15. Jahn U, Gallenberger M, Paper W, Junglas B, Eisenreich W, Stetter KO, Rachel R, Huber H (2008) Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two Archaea. J Bacteriol 190:1743–1750PubMedCrossRefGoogle Scholar
  16. Junglas B, Briegel A, Burghardt T, Walther P, Wirth R, Huber H, Rachel R (2008) Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch Microbiol 190:395–408PubMedCrossRefGoogle Scholar
  17. Kates M (1993) Membrane lipids of Archaea. In: Kates M, Kushner DJ, Matheson AT (eds) The biochemistry of Archaea (Archaebacteria). Elsevier, Amsterdam, pp 261–295CrossRefGoogle Scholar
  18. König H, Rachel R, Claus H (2007) Proteinaceous surface layers of Archaea: ultrastructure and biochemistry. In: Cavicchioli R (ed) Archaea: molecular and cellular biology. ASM Press, Washington, USA, pp 315–340Google Scholar
  19. Küper U, Rachel R, Meyer C, Müller V, Huber H (2010a) Ignicoccus hospitalis und sein Weg ATP zu gewinnen. BIOspektrum 16:628–631Google Scholar
  20. Küper U, Meyer C, Müller V, Rachel R, Huber H (2010b) Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis. Proc Natl Acad Sci USA 107:3152–3156PubMedCrossRefGoogle Scholar
  21. La Scola B, St Audic, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie J-M, Raoult D (2003) A giant virus in amoebae. Science 299:2033PubMedCrossRefGoogle Scholar
  22. Lange M (2009) Neue Hochtemperatur-Organismen von Lesbos und dem Ostpazifischen-Rücken. University of Regensburg, Diploma thesisGoogle Scholar
  23. Lindas A-C, Karlsson EA, Lindgren MT, Ettema TJG, Bernander R (2008) A unique cell division machinery in the Archaea. Proc Natl Acad Sci USA 105:18942–18946PubMedCrossRefGoogle Scholar
  24. Mayer F, Küper U, Meyer C, Daxer S, Müller V, Rachel R, Huber H (2012) An AMP-forming acetyl-CoA synthetase in the outermost membrane of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis. J Bact. doi: 10.1128/JB.06130-11 PubMedGoogle Scholar
  25. Moissl-Eichinger C, Huber H (2011) Archaeal symbionts and parasites. Curr Opin Microbiol 14:1–7CrossRefGoogle Scholar
  26. Müller DW, Meyer C, Gürster S, Küper U, Huber H, Rachel R, Wanner G, Wirth R, Bellack A (2009) The iho670 fibers of Ignicoccus hospitalis: a new type of archaeal cell surface appendage. J Bacteriol 191:6465–6468PubMedCrossRefGoogle Scholar
  27. Näther DJ, Rachel R (2004) The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure and composition. Biochem Soc Trans 32:199–203PubMedCrossRefGoogle Scholar
  28. Näther DJ, Rachel R, Wanner G, Wirth R (2006) Flagella of Pyrococcus furiosus are multifunctional organelles, also serving for surface adhesion and cell cell contacts. J Bacteriol 188:6915–6923PubMedCrossRefGoogle Scholar
  29. Nickell S, Hegerl R, Baumeister W, Rachel R (2003) Pyrodictium cannulae enter the peri-plasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J Struct Biol 141:34–42PubMedCrossRefGoogle Scholar
  30. Paper W, Jahn U, Hohn MJ, Kronner M, Näther DJ, Burghardt T, Rachel R, Stetter KO, Huber H (2007) Ignicoccus hospitalis sp. nov., the host of ‘Nanoarchaeum equitans’. Int J Syst Evol Microbiol 57:803–808PubMedCrossRefGoogle Scholar
  31. Podar M, Anderson I, Makarova KS, Elkins JG, Ivanova N, Wall MA, Lykidis A, Mavromatis K, Sun H, Hudson ME, Chen W, Deciu C, Hutchison D, Eads JR, Anderson A, Fernan-des F, Szeto E, Lapidus A, Kyrpides NC, Saier MH Jr, Richardson PM, Rachel R, Huber H, Eisen JA, Koonin EV, Keller M, Stetter KO (2008a) A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol 9:R158PubMedCrossRefGoogle Scholar
  32. Podar M, Wall MA, Makarova KS, Koonin EV (2008b) The prokaryotic V4R domain is the likely ancestor of a key component of the eukaryotic vesicle transport system. Biol Direct 3:2PubMedCrossRefGoogle Scholar
  33. Rachel R, Wyschkony I, Riehl S, Huber H (2002) The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1:9–18PubMedCrossRefGoogle Scholar
  34. Rachel R, Meyer C, Klingl A, Gürster S, Heimerl T, Wasserburger N, Burghardt T, Küper U, Bellack A, Schopf S, Wirth R, Huber H, Wanner G (2010) Analysis of the ultrastructure of Archaea by electron microscopy. Meth Cell Biol 96:47–69CrossRefGoogle Scholar
  35. Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in Archaea. Science 322:1710–1713PubMedCrossRefGoogle Scholar
  36. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86PubMedCrossRefGoogle Scholar
  37. Thoma C, Frank M, Rachel R, Schmid S, Näther D, Wanner G, Wirth R (2008) The Mth60-fimbriae of Methanothermobacter thermoautotrophicus are functional adhesins. Environ Microbiol 10:2785–2795PubMedCrossRefGoogle Scholar
  38. Vonck J, Pisa KY, Morgner N, Brutschy B, Müller V (2009) Three-dimentional structure of A1Ao ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus by electron microscopy. J Biol Chem 284:10110–10119PubMedCrossRefGoogle Scholar
  39. Waters E, Hohn MJ, Ahel I, Graham DE, Adams MD, Barnstead M, Beeson KY, Bibbs L, Bolanos R, Keller M, Kretz K, Lin X, Mathur E, Ni J, Podar M, Richardson T, Sutton GG, Simon M, Soll D, Stetter KO, Short JM, Noordewier M (2003) The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc Natl Acad Sci USA 100:12984–12988PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Harald Huber
    • 1
  • Ulf Küper
    • 1
    • 3
  • Stefanie Daxer
    • 1
  • Reinhard Rachel
    • 2
  1. 1.Institute for Microbiology and Archaea Center, Faculty of Biology and Preclinical MedicineUniversity RegensburgRegensburgGermany
  2. 2.Faculty of Biology and Preclinical Medicine, Center for Electron MicroscopyUniversity RegensburgRegensburgGermany
  3. 3.BASFLudwigshafenGermany

Personalised recommendations