Respiratory supercomplexes enhance electron transport by decreasing cytochrome c diffusion distance.
bioenergetics
competitive fitness
cryo-EM
mitochondria
respiratory chain supercomplexes
Journal
EMBO reports
ISSN: 1469-3178
Titre abrégé: EMBO Rep
Pays: England
ID NLM: 100963049
Informations de publication
Date de publication:
03 12 2020
03 12 2020
Historique:
received:
02
06
2020
revised:
02
09
2020
accepted:
10
09
2020
pubmed:
6
10
2020
medline:
28
4
2021
entrez:
5
10
2020
Statut:
ppublish
Résumé
Respiratory chains are crucial for cellular energy conversion and consist of multi-subunit complexes that can assemble into supercomplexes. These structures have been intensively characterized in various organisms, but their physiological roles remain unclear. Here, we elucidate their function by leveraging a high-resolution structural model of yeast respiratory supercomplexes that allowed us to inhibit supercomplex formation by mutation of key residues in the interaction interface. Analyses of a mutant defective in supercomplex formation, which still contains fully functional individual complexes, show that the lack of supercomplex assembly delays the diffusion of cytochrome c between the separated complexes, thus reducing electron transfer efficiency. Consequently, competitive cellular fitness is severely reduced in the absence of supercomplex formation and can be restored by overexpression of cytochrome c. In sum, our results establish how respiratory supercomplexes increase the efficiency of cellular energy conversion, thereby providing an evolutionary advantage for aerobic organisms.
Identifiants
pubmed: 33016568
doi: 10.15252/embr.202051015
pmc: PMC7726804
doi:
Substances chimiques
Saccharomyces cerevisiae Proteins
0
Cytochromes c
9007-43-6
Electron Transport Complex IV
EC 1.9.3.1
Banques de données
PDB
['6YMX', '6YMY']
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e51015Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM118141
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2020 The Authors. Published under the terms of the CC BY 4.0 license.
Références
Proc Natl Acad Sci U S A. 2014 Nov 4;111(44):15735-40
pubmed: 25331896
EMBO J. 2020 Jul 15;39(14):e103912
pubmed: 32511785
Mol Cell Biol. 2006 Jul;26(13):4872-81
pubmed: 16782876
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Cell Metab. 2017 Feb 7;25(2):301-311
pubmed: 27916530
EMBO J. 2000 Apr 17;19(8):1777-83
pubmed: 10775262
Cell Metab. 2017 Jan 10;25(1):57-71
pubmed: 28094012
Front Oncol. 2012 Jul 03;2:70
pubmed: 22783546
Elife. 2018 Nov 09;7:
pubmed: 30412051
Mol Cell. 2008 Nov 21;32(4):529-39
pubmed: 19026783
Antioxid Redox Signal. 2013 Dec 1;19(16):1916-27
pubmed: 22703342
Curr Protoc Hum Genet. 2009 Oct;Chapter 19:Unit19.3
pubmed: 19806590
Cell Metab. 2014 Dec 2;20(6):1069-75
pubmed: 25470551
Protein Sci. 2018 Jan;27(1):14-25
pubmed: 28710774
Biochim Biophys Acta Bioenerg. 2020 Jul 1;1861(7):148193
pubmed: 32201307
J Biol Chem. 2004 Aug 27;279(35):36562-9
pubmed: 15205457
J Cell Biol. 2012 Oct 1;199(1):137-50
pubmed: 23007649
Protein Expr Purif. 1999 Apr;15(3):370-80
pubmed: 10092497
Cell Res. 2018 Mar;28(3):281-295
pubmed: 29424373
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Biol Rev Camb Philos Soc. 1966 Aug;41(3):445-502
pubmed: 5329743
Nat Methods. 2017 Mar;14(3):290-296
pubmed: 28165473
J Biol Chem. 2004 Aug 27;279(35):36349-53
pubmed: 15208329
Sci Rep. 2017 Aug 8;7(1):7606
pubmed: 28790391
FASEB J. 2010 May;24(5):1431-41
pubmed: 20008543
Mol Cell. 2019 Jun 6;74(5):877-890.e6
pubmed: 31023583
Yeast. 2004 Aug;21(11):947-62
pubmed: 15334558
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Biol Chem. 2003 Mar 14;278(11):8881-7
pubmed: 12522138
Science. 2013 Jun 28;340(6140):1567-70
pubmed: 23812712
Biochemistry. 1966 Mar;5(3):838-48
pubmed: 4287829
Cell Metab. 2017 Apr 4;25(4):765-776
pubmed: 28380371
Cell Metab. 2018 Sep 4;28(3):525-531.e4
pubmed: 29937372
Cell Metab. 2012 Sep 5;16(3):378-86
pubmed: 22902835
Antioxid Redox Signal. 2013 Nov 1;19(13):1469-80
pubmed: 23581604
Cell Metab. 2012 Mar 7;15(3):324-35
pubmed: 22342700
Nat Struct Mol Biol. 2019 Jan;26(1):78-83
pubmed: 30598554
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Cell Rep. 2016 Aug 30;16(9):2387-98
pubmed: 27545886
Cell Metab. 2018 Jun 05;27(6):1309-1322.e6
pubmed: 29754951
Methods Enzymol. 2002;350:87-96
pubmed: 12073338
Nat Struct Mol Biol. 2019 Jan;26(1):50-57
pubmed: 30598556
Methods Mol Biol. 2006;313:33-9
pubmed: 16118422
EMBO Rep. 2020 Dec 3;21(12):e51015
pubmed: 33016568
Cell Rep. 2020 May 5;31(5):107607
pubmed: 32375044
Semin Cell Dev Biol. 2018 Apr;76:179-190
pubmed: 28743641
EMBO Rep. 2020 Jul 3;21(7):e50287
pubmed: 32496654
Acta Crystallogr D Struct Biol. 2019 Oct 1;75(Pt 10):861-877
pubmed: 31588918
Mol Cell. 2004 Mar 26;13(6):805-15
pubmed: 15053874
Methods Mol Biol. 2008;457:125-39
pubmed: 19066023
J Cell Biol. 2011 Jun 13;193(6):1101-14
pubmed: 21670217
Cell Rep. 2018 Nov 13;25(7):1786-1799.e4
pubmed: 30428348
J Cell Biol. 2017 Dec 4;216(12):3917-3929
pubmed: 29167179
BMC Biol. 2018 Nov 1;16(1):111
pubmed: 30382836
J Cell Biol. 2014 May 26;205(4):511-24
pubmed: 24841564
J Biol Chem. 2002 Nov 15;277(46):43553-6
pubmed: 12364341
Front Mol Neurosci. 2018 Jun 21;11:205
pubmed: 29977190
Cell Metab. 2017 Jan 10;25(1):128-139
pubmed: 27720676
Biochim Biophys Acta. 2014 Apr;1837(4):444-50
pubmed: 24368156
Proc Natl Acad Sci U S A. 2011 Nov 8;108(45):E1027-34
pubmed: 22011573