The unusual cell biology of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis
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.
KeywordsIgnicoccus 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.).
- 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
- Daxer S (2011) Lokalisation stoffwechselrelevanter Enzymkomplexe sowie Anreicherung einer membrangebundenen Pyrophosphatase in Vertretern der archaeellen Gattung Ignicoccus. University of Regensburg, Master thesisGoogle Scholar
- 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
- 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. www.prokaryotes.com
- 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
- 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
- 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
- Küper U, Rachel R, Meyer C, Müller V, Huber H (2010a) Ignicoccus hospitalis und sein Weg ATP zu gewinnen. BIOspektrum 16:628–631Google Scholar
- Lange M (2009) Neue Hochtemperatur-Organismen von Lesbos und dem Ostpazifischen-Rücken. University of Regensburg, Diploma thesisGoogle Scholar
- 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
- 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