Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 30; pp. 8442 - 8447
• Main Authors: Mühleip, Alexander W., Joos, Friederike, Wigge, Christoph, Frangakis, Achilleas S., Kühlbrandt, Werner, Davies, Karen M.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 26.07.2016
• Subjects: Adenosine diphosphate; Adenosine triphosphatase; Animals; Arrays; ATP; Biological Sciences; Mammals; Microscopy, Electron; Mitochondria; Mitochondria - metabolism; Mitochondria - ultrastructure; Mitochondrial Membranes - metabolism; Mitochondrial Membranes - ultrastructure; Mitochondrial Proton-Translocating ATPases - chemistry; Mitochondrial Proton-Translocating ATPases - metabolism; Models, Molecular; Paramecium tetraurelia; Paramecium tetraurelia - enzymology; Paramecium tetraurelia - metabolism; Paramecium tetraurelia - ultrastructure; Protein Conformation; Protein Multimerization; Protein Structure, Secondary; Protozoan Proteins - chemistry; Protozoan Proteins - metabolism; Yeast; Yeasts; subtomogram averaging; cryoelectron microscopy; serial block face imaging; macromolecular organization; Paramecium
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1525430113

F₁Fₒ-ATP synthases are universal energy-converting membrane protein complexes that synthesize ATP from ADP and inorganic phosphate. In mitochondria of yeast and mammals, the ATP synthase forms V-shaped dimers, which assemble into rows along the highly curved ridges of lamellar cristae. Using electron cryotomography and subtomogram averaging, we have determined the in situ structure and organization of the mitochondrial ATP synthase dimer of the ciliate Paramecium tetraurelia. The ATP synthase forms U-shaped dimers with parallel monomers. Each complex has a prominent intracrista domain, which links the c-ring of one monomer to the peripheral stalk of the other. Close interaction of intracrista domains in adjacent dimers results in the formation of helical ATP synthase dimer arrays, which differ from the loose dimer rows in all other organisms observed so far. The parameters of the helical arrays match those of the cristae tubes, suggesting the unique features of the P. tetraurelia ATP synthase are directly responsible for generating the helical tubular cristae. We conclude that despite major structural differences between ATP synthase dimers of ciliates and other eukaryotes, the formation of ATP synthase dimer rows is a universal feature of mitochondria and a fundamental determinant of cristae morphology.