Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals.

Chimari Jiko,Shintaro Maeda,Christoph Gerle,Tomitake Tsukihara,Kazutoshi Tani,Deryck J Mills,Kyoko Shinzawa-Itoh,Karen M Davies,Yoshinori Fujiyoshi,Werner Kühlbrandt

doi:10.7554/elife.06119

Abstract

We have used a combination of electron cryo-tomography, subtomogram averaging, and electron crystallographic image processing to analyse the structure of intact bovine F(1)F(o) ATP synthase in 2D membrane crystals. ATPase assays and mass spectrometry analysis of the 2D crystals confirmed that the enzyme complex was complete and active. The structure of the matrix-exposed region was determined at 24 Å resolution by subtomogram averaging and repositioned into the tomographic volume to reveal the crystal packing. F(1)F(o) ATP synthase complexes are inclined by 16° relative to the crystal plane, resulting in a zigzag topology of the membrane and indicating that monomeric bovine heart F(1)F(o) ATP synthase by itself is sufficient to deform lipid bilayers. This local membrane curvature is likely to be instrumental in the formation of ATP synthase dimers and dimer rows, and thus for the shaping of mitochondrial cristae.

Highlights

The F1Fo ATP synthase is a membrane-embedded nano-machine and a member of the rotary ATPases (F, V- and A-ATPases), which are found in energy-converting membranes of all eukaryotes, bacteria, and archaea (Muench et al, 2011)
The enzyme can be subdivided into four essential functional parts: the catalytic part,3, which binds and converts ADP and Pi to ATP; the membraneembedded part (a, b, c8, e, f, g, A6L, DAPIT, and the 6.8 kDa protein) through which protons move across the membrane; the central stalk, γδε, which transmits the rotation of the membrane-embedded rotor-ring (c8) to the catalytic region; and the peripheral stalk (b, d, F6 and OSCP) which holds the catalytic part stationary relative to the membrane region
Our results demonstrate that the transmembrane region of bovine mitochondrial F1Fo ATP synthase monomer is sufficient to bend the lipid bilayer

Summary

Introduction

The F1Fo ATP synthase is a membrane-embedded nano-machine and a member of the rotary ATPases (F-, V- and A-ATPases), which are found in energy-converting membranes of all eukaryotes, bacteria, and archaea (Muench et al, 2011). The enzyme can be subdivided into four essential functional parts: the catalytic part, (αβ), which binds and converts ADP and Pi to ATP; the membraneembedded part (a, b, c8, e, f, g, A6L, DAPIT, and the 6.8 kDa protein) through which protons move across the membrane; the central stalk, γδε, which transmits the rotation of the membrane-embedded rotor-ring (c8) to the catalytic region; and the peripheral stalk (b, d, F6 and OSCP) which holds the catalytic part stationary relative to the membrane region. A number of atomic models have been obtained by x-ray crystallography for various parts of the yeast and bovine mitochondrial F1Fo ATP synthase including the F1 subcomplex (Abrahams et al, 1994), the F1/c-ring subcomplex (Stock et al, 1999; Watt et al, 2010), the peripheral stalk subcomplex (Dickson et al, 2006), and the

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Conclusion