Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism.
Adaptation, Physiological
/ radiation effects
Adenosine Triphosphate
/ metabolism
Benzoquinones
/ metabolism
Cell Membrane
/ metabolism
Cells
/ metabolism
Chromatophores
/ metabolism
Cytochromes c2
/ metabolism
Diffusion
Electron Transport
/ radiation effects
Energy Metabolism
/ radiation effects
Environment
Hydrogen Bonding
Kinetics
Light
Molecular Dynamics Simulation
Phenotype
Proteins
/ metabolism
Rhodobacter sphaeroides
/ physiology
Static Electricity
Stress, Physiological
/ radiation effects
Temperature
MD
bioenergetics
biological membranes
charge transport
chromatophore
integrative model
mitochondria
molecular dynamics simulation
optical spectroscopy
photosynthesis
Journal
Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066
Informations de publication
Date de publication:
14 11 2019
14 11 2019
Historique:
received:
27
03
2019
revised:
04
09
2019
accepted:
21
10
2019
entrez:
16
11
2019
pubmed:
16
11
2019
medline:
27
5
2020
Statut:
ppublish
Résumé
We report a 100-million atom-scale model of an entire cell organelle, a photosynthetic chromatophore vesicle from a purple bacterium, that reveals the cascade of energy conversion steps culminating in the generation of ATP from sunlight. Molecular dynamics simulations of this vesicle elucidate how the integral membrane complexes influence local curvature to tune photoexcitation of pigments. Brownian dynamics of small molecules within the chromatophore probe the mechanisms of directional charge transport under various pH and salinity conditions. Reproducing phenotypic properties from atomistic details, a kinetic model evinces that low-light adaptations of the bacterium emerge as a spontaneous outcome of optimizing the balance between the chromatophore's structural integrity and robust energy conversion. Parallels are drawn with the more universal mitochondrial bioenergetic machinery, from whence molecular-scale insights into the mechanism of cellular aging are inferred. Together, our integrative method and spectroscopic experiments pave the way to first-principles modeling of whole living cells.
Identifiants
pubmed: 31730852
pii: S0092-8674(19)31171-7
doi: 10.1016/j.cell.2019.10.021
pmc: PMC7075482
mid: NIHMS1553648
pii:
doi:
Substances chimiques
Benzoquinones
0
Proteins
0
quinone
3T006GV98U
Adenosine Triphosphate
8L70Q75FXE
Cytochromes c2
9035-43-2
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
1098-1111.e23Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M000265/1
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : P41 GM104601
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM067887
Pays : United States
Organisme : European Research Council
Pays : International
Commentaires et corrections
Type : CommentIn
Informations de copyright
Published by Elsevier Inc.
Références
Cell. 2012 Jul 20;150(2):389-401
pubmed: 22817898
Biochemistry. 2013 Oct 29;52(43):7575-85
pubmed: 24131108
EMBO J. 1999 Feb 1;18(3):534-42
pubmed: 9927413
J Phys Chem B. 2016 Nov 10;120(44):11449-11463
pubmed: 27723973
J Comput Chem. 2005 Dec;26(16):1781-802
pubmed: 16222654
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9360-2
pubmed: 10944207
Biochemistry. 2005 Aug 23;44(33):10994-1004
pubmed: 16101283
J Biol Chem. 2008 Sep 5;283(36):24826-36
pubmed: 18617515
Mol Microbiol. 2012 Jun;84(6):1062-78
pubmed: 22621241
J Phys Chem B. 2017 Apr 20;121(15):3787-3797
pubmed: 28301162
J Biol Chem. 2008 Nov 7;283(45):30772-9
pubmed: 18723509
Biophys J. 2010 Jul 7;99(1):67-75
pubmed: 20655834
Biochim Biophys Acta Bioenerg. 2018 Mar;1859(3):215-225
pubmed: 29291373
Sci Rep. 2017 Nov 22;7(1):16078
pubmed: 29167583
Elife. 2016 Aug 26;5:
pubmed: 27564854
Cell. 2005 Jun 3;121(5):671-4
pubmed: 15935754
Annu Rev Biophys. 2016 Jul 5;45:253-78
pubmed: 27145875
J Am Chem Soc. 2017 Jan 11;139(1):293-310
pubmed: 27936329
J Am Chem Soc. 2016 Sep 21;138(37):12077-89
pubmed: 27508459
Cell. 2015 Apr 23;161(3):450-457
pubmed: 25910205
Biochim Biophys Acta. 2014 Oct;1837(10):1769-80
pubmed: 24530865
Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15723-8
pubmed: 17895378
PLoS Comput Biol. 2014 Jul 17;10(7):e1003720
pubmed: 25032790
Proc Natl Acad Sci U S A. 2017 Apr 11;114(15):3790-3791
pubmed: 28360203
J Phys Chem B. 2010 Sep 30;114(38):12427-37
pubmed: 20809619
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41
pubmed: 11517324
Biochim Biophys Acta. 2012 Sep;1817(9):1616-27
pubmed: 22659614
Biophys J. 2008 Sep 15;95(6):2822-36
pubmed: 18515401
J Biol Chem. 2005 Mar 25;280(12):11214-23
pubmed: 15632163
PLoS One. 2010 Nov 22;5(11):e14070
pubmed: 21124924
FEBS Lett. 1998 Apr 10;426(1):77-80
pubmed: 9598982
Chem Rev. 2015 Mar 11;115(5):2196-221
pubmed: 25694135
Mol Microbiol. 2018 Sep;109(6):812-825
pubmed: 29995992
J Biol Chem. 2008 May 16;283(20):14002-11
pubmed: 18326046
Photosynth Res. 2014 May;120(1-2):169-80
pubmed: 23539360
Chem Sci. 2018 Feb 9;9(12):3095-3104
pubmed: 29732092
Biophys J. 2014 Jun 3;106(11):2503-10
pubmed: 24896130
J Chem Phys. 2007 Sep 28;127(12):125101
pubmed: 17902937
Plant Methods. 2013 Jul 22;9:29
pubmed: 23876160
Nat Methods. 2006 Oct;3(10):793-5
pubmed: 16896339
Adv Exp Med Biol. 2010;675:161-78
pubmed: 20532741
ACS Nano. 2017 Jan 24;11(1):126-133
pubmed: 28114766
Nature. 1990 Oct 18;347(6294):631-9
pubmed: 2215695
J Phys Chem C Nanomater Interfaces. 2012 Feb 9;116(5):3376-3393
pubmed: 22606364
Biophys J. 2007 Jan 1;92(1):23-33
pubmed: 17028136
Nature. 2016 Sep 29;537(7622):644-648
pubmed: 27654913
Annu Rev Physiol. 2004;66:689-733
pubmed: 14977419
Biochemistry. 1999 Dec 21;38(51):16866-75
pubmed: 10606520
Biophys J. 2013 Jul 16;105(2):343-55
pubmed: 23870256
J Phys Chem B. 2007 Jul 12;111(27):7812-24
pubmed: 17569554
J Biol Chem. 2004 May 14;279(20):21327-33
pubmed: 14993213
J Biol Chem. 2005 Mar 25;280(12):11203-13
pubmed: 15632164