Bioenergetics: New features of ATP synthase
2021-01-08
(Press-News.org) The mitochondrial ATP synthase is energy-converting macromolecular machine that uses the electrochemical potential across the bioenergetic membrane called cristae. This potential is maintained via a membrane curvature that is induced by ATP synthase assembled in dimers. The dimers shaping the bioenergetic membrane were thought to be universal across the eukaryotic organisms. Two newly published cryo-EM studies by Kock-Flygaard et al and Mühleip et al from Alexey Amunts lab, identify different types of ATP synthase organization.
The structure of the ATP synthase from ciliates revealed a dimer, which unlike in all the previously investigated complexes, the two membrane-embedded parts are not identical to each other. The commonly observed symmetry is broken by the accommodation of a single subunit at the dimer interface that anchors an inhibitor. In addition, the ATP synthase has an unusual U-shape arrangement, and thus the generation of the membrane curvature is achieved through tetramerization. Therefore, this work defines ATP synthase tetramer as the intact structural unit propagating cristae formation in ciliates.
The investigation of the infectious apicomplexan parasites Toxoplasma, revealed that their ATP synthase is arranged in cyclic hexamers. However, within the hexamer, the lipid bilayer turns out to be near-planar, which is not sufficient to shape the bioenergetic membrane. Therefore, the cryo-electron tomography approach was applied to the native membranes isolated from the parasites' mitochondria, which revealed that the hexamers are further arranged in a higher order of organization. Particularly, 20 units of ATP synthase are linked together in large arrays with icosahedral symmetry. They form pentagonal pyramids at the size of 20 mega-Dalton. In the center of each pyramid, hexamer ATP synthase planes are oriented by 40°. Therefore, the mechanism of pentagonal pyramids generates cristae morphology in a way that differs from the canonical dimers thought to be universal.
Finally, the structural studies identified a key subunit ATPTG11 holding the hexamers together. A removal of the subunit showed loss of pentagonal pyramids, aberrantly shaped cristae, and defective growth of the parasites. This demonstrates that the unique macromolecular arrangement is critical for the maintenance of bioenergetics in Apicomplexa.
Together, these studies illustrate the structural basis for the diversity of the membrane-shaping properties of mitochondrial ATP synthases. This suggests that the fundamental mechanism of the ATP synthase association varies between eukaryotic lineages.
INFORMATION:
References:
Flygaard RK, Mühleip A, Tobiasson V, Amunts A. Type III ATP synthase is a symmetry-deviated dimer that induces membrane curvature through tetramerization. Nature communications. 2020; 11.
Muhleip A, Kock Flygaard R, Ovciarikova J, Lacombe A, Fernandes P, Sheiner L, Amunts A. ATP synthase hexamer assemblies shape cristae of Toxoplasma mitochondria. Nature communications. 2021; 12.
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[Press-News.org] Bioenergetics: New features of ATP synthase
