Structural biology of mitochondria. Werner Kühlbrandt Max Planck Institute of Biophysics Frankfurt, Germany

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1 Structural biology of mitochondria Werner Kühlbrandt Max Planck Institute of Biophysics Frankfurt, Germany

2 The mitochondrion Powerhouse of the eukaryotic cell Produces almost all ATP to drive cellular reactions Semi-autonomous cell organelle (division, fusion, own genetic system) Imports > 99% of proteins from cytoplasm Outer membrane is permeable to small molecules Inner membrane is site of respiration and ATP synthesis Major role in ageing and apoptosis

3 Schematic drawing of mitochondrion outer membrane outer membrane intermembrane space ph 7.35 inner membrane matrix ph 7.9 ~ 2000 different proteins cristae > 99% produced outside ~500 nm

4 Mitochondria in a human endothelial cell QuickTime and a decompressor are needed to see this picture. ~10 µm Jürgen Bereiter-Hahn, Frankfurt University

5 Podospora anserina has smaller mitochondria with fewer cristae cristae junctions cristae ridges Bertram Daum

6 Arrangement of the mitochondrial ATP synthase

7 The mitochondrial respiratory chain ADP + Pi NADH ATP NAD+ succinate O2 H + 2H2O matrix UQ UQ cristae space H + Complex I NADH dehydrogenase H cytochrome c + H + H + Complex III Complex II Complex IV cytochrome c succinate cytochrome c oxidase reductase dehydrogenase drawn by Karen Davies + H H + Complex V ATP synthase

8 Deep-etched Paramecium mitochondrion 200 nm R.D.Allen et al, J.Cell Biol. 1989

9 Dimer ribbons in mammalian mitochondria 20 nm rat liver: tubular cristae bovine heart: lamellar cristae Strauss et al, EMBO J 2008

10 Dimer rows are ubiquitous lipolytica Polytomella subtomogram averages Karen Davies

11 Cryo-ET of Podospora mitochondrion ATP synthase dimers QuickTime and a decompressor are needed to see this picture. ribosomes inner membrane Davies et al, PNAS 2011

12 Sub-tomogram average of yeast dimer Davies et al, PNAS 2012

13 Resolution estimate average of 121 sub-tomograms 3.7 nm Davies et al, PNAS 2012

14 Sub-tomogram average of ATP synthase dimer F1 head peripheral stalk central stalk rotor ring Davies et al, PNAS 2012

15 Sub-tomogram average of ATP synthase dimer F1 head peripheral stalk beta subunits Davies et al, PNAS 2012

16 Fit of peripheral stalk bovine F1/peripheral stalk (2WSS; Rees et al, PNAS 2009) yeast F1/Fo+bovine peripheral stalk (2CLY; Dickson et al, EMBO J 2006) Davies et al, PNAS 2012

17 ATP synthase dimers self-organize into rows coarse-grained MD simulation by José Faraldo-Gomez, Claudio Anselmi, MPI of Biophysics Davies et al, PNAS 2012

18 Free energy of dimer association Energy of elastic membrane deformation is > 6 kt per dimer For comparison: Free energy of protein-protein interaction (glycophorin A dimer) ~15 kt José Faraldo-Gomez, Claudio Anselmi, MPI of Biophysics Davies et al, PNAS 2012

19 ATP synthase monomers stroma ~ ph 8 thylakoid lumen ~ ph 5 thylakoid membrane inner membrane outer membrane Chloropla

20 ATP synthesis in chloroplasts maximal rate ~400 ATP per synthase per second at a delta ph of 2.5 and a membrane potential of 55 mv 2.5 Junesch and Gräber, FEBS Lett 1991

21 ATP synthesis in mitochondria maximal rate ~80 ATP per synthase per second cristae ph 5.0?? at a delta ph of 2.9 and a membrane potential of 133 mv 2.5 matrix ph 7.9 Förster, Turina, Drepper, Hähnel, Fischer, Gräber, Petersen, BBA 2010

22 subunits e, g, 4 respiratory chain proton pumps (complex I, III, IV) ATP synthase dimers matrix: ph 7.9 inner membrane outer membrane ph intermembrane space = ph cytoplasm: 7.35 Mitochond

23 Respiratory chain supercomplex

24 The mitochondrial respiratory chain ADP + Pi NADH ATP NAD+ succinate O2 H + 2H2O matrix UQ UQ cristae space H + Complex I NADH dehydrogenase H cytochrome c + H + H + Complex III Complex II Complex IV cytochrome c succinate cytochrome c oxidase reductase dehydrogenase drawn by Karen Davies + H H + Complex V ATP synthase

25 Podospora cristae vesicle ATP synthase dimer row 1 QuickTime and a decompressor are needed to see this picture. ATP synthase dimer row 2 respiratory chain complexes crista membrane Davies et al, PNAS 2011

26 Supercomplex in cristae membranes quantum-dot labelled complex I supercomplex next to dimer row Davies et al, PNAS 2011

27 Respiratory chain supercomplex I1II2IV1 random conical tilt on thin C film class averages reprojections of final volume Althoff et al, EMBO J 2011

28 3D cryo-em map amphipol ring Althoff et al, EMBO J 2011

29 Respiratory chain supercomplex I1II2IV1 complex I (NADH UQ oxidoreductase) Hunte, Zickermann et al, 2010 complex III2 (cytochrome c reductase) Hunte et al, 2000 complex IV (cytochrome c oxidase) Tsukihara et al, 1996 cytochrome c Rieske FeS membrane 50 Å Althoff et al, EMBO J 2011

30 10 nm

31 Electron transfer pathways complex I to complex III: UQ complex III to complex IV: cyt c Althoff et al, EMBO J 2011

32 Sites of oxygen radical production

33 Protein import

34 Cryo-ET of chloroplast protein translocase a b c d 15 nm e f 15 nm Bertram Daum with Enrico Schleiff, Frankfurt; Sommer et al, PNAS 2011

35 Quantum dot labelling of TOC subunits a 15 nm cytoplasmic location of TOC receptor GTPase α-75p α-34g b 15 nm α-75p Bertram Daum with Enrico Schleiff, Frankfurt; Sommer et al, PNAS 2011 cytoplasmic location of TOC75 POTRA domain

36 Ageing

37 Podospora anserina: filamentous fungus with a fixed lifespan hyphae filamentous, multicellular fungus fixed lifespan of ~20 days long-lived and immortal mutants culture 9 days 18 days (senescent) from Scheckhuber et al, 2006 mitochondria 6 days 18 days (juvenile) (senescent)

38 Age-dependent change of mitochondria young (6 days) P. anserina Bertram Daum with Heinz Osiewacz, Frankfurt old (18 days)

39 Dimer-specific subunit knockouts cristae morphology ATP synthase arrangement wild type yeast dimer rows along edges subunit g knockout randomly distributed monomers Davies et al, PNAS 2012

40 Single-particle team Doreen Mathies Deryck Mills Janet Vonck Thorsten Althoff

41 X-ray structure of CaiT Electron tomography team Bertram Deryck Mills Daum Karen Davies Thorsten Blum

42 Open V13? close V12? close V8? make a coffee? fill with LN2? have breakfast? turn up HT? water plants? turn on dryer? EM? (check notes) go home? How to fix it if it gets broken by Deryck First & last edition

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