Energized Outer Membrane and Spatial Separation of Metabolic Processes in the Hyperthermophilic Archaeon Ignicoccus Hospitalis

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 107; no. 7; pp. 3152 - 3156
• Main Authors: Küper, Ulf, Meyer, Carolin, Müller, Volker, Rachel, Reinhard, Huber, Harald, Soil, Dieter
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 16.02.2010; National Acad Sciences
• Subjects: Adenosine triphosphatase; Adenosine triphosphatases; Adenosine Triphosphate - biosynthesis; Antibodies; Archaea; ATP Synthetase Complexes - metabolism; Biological Sciences; Catalysis; Cell membranes; Cells; Cytoplasm; Desulfurococcaceae; Desulfurococcaceae - metabolism; Desulfurococcaceae - ultrastructure; Electrophoresis; Enzymes; Fluorescent Antibody Technique; Gels; Membranes; Metabolism; Microorganisms; Microscopy, Fluorescence; Microscopy, Immunoelectron; Oxidoreductases Acting on Sulfur Group Donors - metabolism; P branes; Periplasm; Periplasmic Proteins - metabolism; Protein synthesis
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0911711107

ATP synthase catalyzes ATP synthesis at the expense of an electrochemical ion gradient across a membrane that can be generated by different exergonic reactions. Sulfur reduction is the main energyyielding reaction in the hyperthermophilic strictly anaerobic Crenarchaeon Ignicoccus hospitalis. This organism is unusual in having an inner and an outer membrane that are separated by a huge intermembrane compartment. Here we show, on the basis of immuno-EM analyses of ultrathin sections and immunof luorescence experiments with whole l. hospitalis cells, that the ATP synthase and H ₂ : sulfur oxidoreductase complexes of this organism are located in the outer membrane. These two enzyme complexes are mandatory for the generation of an electrochemical gradient and for ATP synthesis. Thus, among all prokaryotes possessing two membranes in their cell envelope (including Planctomycetes, Gram-negative bacteria), l. hospitalis is a unique organism, with an energized outer membrane and ATP synthesis within the periplasmic space. In addition, DAPI staining and EM analyses showed that DNA and ribosomes are localized in the cytoplasm, leading to the conclusion that in l. hospitalis energy conservation is separated from information processing and protein biosynthesis. This raises questions regarding the function of the two membranes, the interaction between these compartments, and the general definition of a cytoplasmic membrane.