Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism

Abhishek Singharoy; Christopher Maffeo; Karelia H. Delgado-Magnero; David J.K. Swainsbury; Melih Sener; Ulrich Kleinekathöfer; John W. Vant; Jonathan Nguyen; Andrew Hitchcock; Barry Isralewitz; Ivan Teo; Danielle E. Chandler; John E. Stone; James C. Phillips; Taras V. Pogorelov; M. Ilaria Mallus; Christophe Chipot; Zaida Luthey-Schulten; D. Peter Tieleman; C. Neil Hunter; Emad Tajkhorshid; Aleksei Aksimentiev; Klaus Schulten

doi:10.1016/j.cell.2019.10.021

Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism

Abhishek Singharoy, Christopher Maffeo, Karelia H. Delgado-Magnero, David J.K. Swainsbury, Melih Sener, Ulrich Kleinekathöfer, John W. Vant, Jonathan Nguyen, Andrew Hitchcock, Barry Isralewitz, Ivan Teo, Danielle E. Chandler, John E. Stone, James C. Phillips, Taras V. Pogorelov, M. Ilaria Mallus, Christophe Chipot, Zaida Luthey-Schulten, D. Peter Tieleman, C. Neil HunterEmad Tajkhorshid, Aleksei Aksimentiev, Klaus Schulten

Research output: Contribution to journal › Article › peer-review

123 Scopus citations

Abstract

A full atomic resolution model of an entire organelle, the photosynthetic chromatophore vesicle of a purple bacterium, is constructed and reveals how the photosynthetic apparatus is optimized for ATP production in low-light habitats.

Original language	English
Pages (from-to)	1098-1111.e23
Journal	Cell
Volume	179
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2019.10.021
State	Published - Nov 14 2019
Externally published	Yes

Funding

A.S. acknowledges start-up award funds from Arizona State University and grants from the Research Corporation for Science Advancement and the Gordon and Betty Moore Foundation; United States , Lightworks Foundation , and Flinn Foundation . E.T., A.A., C.M., A.S., C.C., B.I., I.T., D.C., J.E.S., and J.P. acknowledge NIH grants P41-GM104601 (PI: E.T.) and NIH R01-GM067887 (PI: E.T.). A.S., C.M., Z.L.-S., and A.A. acknowledge the Center for Physics of Living Cells ( NSF PHY-1430124 ). M.S. and Z.L.-S. also acknowledge NSF funding through MCB1616790 . T.V.P. acknowledges support from the Department of Chemistry , the School of Chemical Sciences , and the Office of the Vice Chancellor for Research at the University of Illinois at Urbana-Champaign . C.C. acknowledges support from the Contrat Plan État Région (CPER) IT2MP and the European Regional Development Fund (ERDF). Work in D.P.T.’s group is supported by the Natural Sciences and Engineering Research Council (Canada) with further support from the Canada Research Chairs Program and Alberta Innovates Technology Futures . D.P.T. and K.H.D.M. acknowledge Compute Canada , funded by the Canada Foundation of Innovation and partners, for computational resources. U.K. acknowledges grant KL 1299/12-1 from the Deutsche Forschungsgemeinschaft (DFG). D.J.K.S., A.H., and C.N.H. acknowledge research grant BB/M000265/1 from the Biotechnology and Biological Sciences Research Council (UK). C.N.H. was also supported by advanced award 338895 from the European Research Council . The study was also funded by the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center supported by the Department of Energy , Office of Science , and Office of Basic Energy Sciences under award DE-SC0001035 (to C.N.H., K.S., and M.S.). This research used resources of the Oak Ridge Leadership Computing Facility, which is supported by the Office of Science , Department of Energy ( DE-AC05-00OR22725 ). A.S. acknowledges start-up award funds from Arizona State University and grants from the Research Corporation for Science Advancement and the Gordon and Betty Moore Foundation; United States, Lightworks Foundation, and Flinn Foundation. E.T. A.A. C.M. A.S. C.C. B.I. I.T. D.C. J.E.S. and J.P. acknowledge NIH grants P41-GM104601 (PI: E.T.) and NIH R01-GM067887 (PI: E.T.). A.S. C.M. Z.L.-S. and A.A. acknowledge the Center for Physics of Living Cells (NSF PHY-1430124). M.S. and Z.L.-S. also acknowledge NSF funding through MCB1616790. T.V.P. acknowledges support from the Department of Chemistry, the School of Chemical Sciences, and the Office of the Vice Chancellor for Research at the University of Illinois at Urbana-Champaign. C.C. acknowledges support from the Contrat Plan ?tat R?gion (CPER) IT2MP and the European Regional Development Fund (ERDF). Work in D.P.T.?s group is supported by the Natural Sciences and Engineering Research Council (Canada) with further support from the Canada Research Chairs Program and Alberta Innovates Technology Futures. D.P.T. and K.H.D.M. acknowledge Compute Canada, funded by the Canada Foundation of Innovation and partners, for computational resources. U.K. acknowledges grant KL 1299/12-1 from the Deutsche Forschungsgemeinschaft (DFG). D.J.K.S. A.H. and C.N.H. acknowledge research grant BB/M000265/1 from the Biotechnology and Biological Sciences Research Council (UK). C.N.H. was also supported by advanced award 338895 from the European Research Council. The study was also funded by the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center supported by the Department of Energy, Office of Science, and Office of Basic Energy Sciences under award DE-SC0001035 (to C.N.H. K.S. and M.S.). This research used resources of the Oak Ridge Leadership Computing Facility, which is supported by the Office of Science, Department of Energy (DE-AC05-00OR22725). Conceptualization, A.S. A.A. M.S. C.N.H. and K.S.; Methodology, A.S. M.S. C.M. A.A. U.K. C.C. D.P.T. Z.L.-S. and C.N.H.; Investigation, A.S. C.M. K.H.D.M. D.J.K.S. M.S. U.K. J.W.V. J.N. I.T. D.E.C. A.H. T.V.P. and M.I.M.; Writing ? Original Draft, A.S. A.A. K.H.D.M. M.S. C.C. Z.L.-S. E.T. and C.N.H.; Writing ? Review & Editing, J.W.V. J.N. A.S. A.A. C.C. K.H.D.M. M.S. U.K. D.P.T. E.T. D.J.K.S. and A.H.; Visualization, B.I. J.E.S. and A.S.; Funding Acquisition, A.S. E.T. Z.L.-S. A.A. and K.S.; Resources, A.S. J.C.P. J.E.S. A.A. Z.L.-S. and E.T.; Supervision, A.S. A.A. C.N.H. D.P.T. and K.S. The authors declare no competing interests.

Funders	Funder number
A.H.
C.C.
Contrat Plan ?
Contrat Plan État Région
Department of Chemistry
Energy Frontier Research Center
J.W.V.
Lightworks Foundation
M.S. U.K.
M.S. U.K. D.P.T. E.T.
NIH R01-GM067887	NSF PHY-1430124, R01-GM067887
Oak
Office of Basic Energy Sciences	DE-SC0001035
Office of Science , Department of Energy	DE-AC05-00OR22725
Office of Science, Department of Energy
Photosynthetic Antenna Research Center
School of Chemical Sciences
U.K.	KL 1299/12-1
U.K. C.C. D.P.T. Z.L.-S
National Institutes of Health	P41-GM104601
National Institutes of Health
U.S. Department of Energy
National Institute of General Medical Sciences	R01GM067887
National Institute of General Medical Sciences
Gordon and Betty Moore Foundation
Flinn Foundation
Research Corporation for Science Advancement
National Sleep Foundation	MCB1616790
National Sleep Foundation
University of Illinois at Urbana-Champaign
Office of Science
Office of the Vice Chancellor for Research, University of Illinois at Urbana-Champaign
Arizona State University
National Council for Eurasian and East European Research
Compute Canada
M.S.I. Foundation
Natural Sciences and Engineering Research Council of Canada
Alberta Innovates - Technology Futures
Canada Foundation for Innovation
Biotechnology and Biological Sciences Research Council	BB/M000265/1, 338895
Biotechnology and Biological Sciences Research Council
Deutsche Forschungsgemeinschaft
European Regional Development Fund

Keywords

MD
bioenergetics
biological membranes
charge transport
chromatophore
integrative model
mitochondria
molecular dynamics simulation
optical spectroscopy
photosynthesis

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10.1016/j.cell.2019.10.021

Cite this

Singharoy, A., Maffeo, C., Delgado-Magnero, K. H., Swainsbury, D. J. K., Sener, M., Kleinekathöfer, U., Vant, J. W., Nguyen, J., Hitchcock, A., Isralewitz, B., Teo, I., Chandler, D. E., Stone, J. E., Phillips, J. C., Pogorelov, T. V., Mallus, M. I., Chipot, C., Luthey-Schulten, Z., Tieleman, D. P., ... Schulten, K. (2019). Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism. Cell, 179(5), 1098-1111.e23. https://doi.org/10.1016/j.cell.2019.10.021

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title = "Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism",

abstract = "A full atomic resolution model of an entire organelle, the photosynthetic chromatophore vesicle of a purple bacterium, is constructed and reveals how the photosynthetic apparatus is optimized for ATP production in low-light habitats.",

keywords = "MD, bioenergetics, biological membranes, charge transport, chromatophore, integrative model, mitochondria, molecular dynamics simulation, optical spectroscopy, photosynthesis",

author = "Abhishek Singharoy and Christopher Maffeo and Delgado-Magnero, {Karelia H.} and Swainsbury, {David J.K.} and Melih Sener and Ulrich Kleinekath{\"o}fer and Vant, {John W.} and Jonathan Nguyen and Andrew Hitchcock and Barry Isralewitz and Ivan Teo and Chandler, {Danielle E.} and Stone, {John E.} and Phillips, {James C.} and Pogorelov, {Taras V.} and Mallus, {M. Ilaria} and Christophe Chipot and Zaida Luthey-Schulten and Tieleman, {D. Peter} and Hunter, {C. Neil} and Emad Tajkhorshid and Aleksei Aksimentiev and Klaus Schulten",

note = "Publisher Copyright: {\textcopyright} 2019",

year = "2019",

month = nov,

day = "14",

doi = "10.1016/j.cell.2019.10.021",

language = "English",

volume = "179",

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journal = "Cell",

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Singharoy, A, Maffeo, C, Delgado-Magnero, KH, Swainsbury, DJK, Sener, M, Kleinekathöfer, U, Vant, JW, Nguyen, J, Hitchcock, A, Isralewitz, B, Teo, I, Chandler, DE, Stone, JE, Phillips, JC, Pogorelov, TV, Mallus, MI, Chipot, C, Luthey-Schulten, Z, Tieleman, DP, Hunter, CN, Tajkhorshid, E, Aksimentiev, A & Schulten, K 2019, 'Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism', Cell, vol. 179, no. 5, pp. 1098-1111.e23. https://doi.org/10.1016/j.cell.2019.10.021

TY - JOUR

T1 - Atoms to Phenotypes

T2 - Molecular Design Principles of Cellular Energy Metabolism

AU - Singharoy, Abhishek

AU - Maffeo, Christopher

AU - Delgado-Magnero, Karelia H.

AU - Swainsbury, David J.K.

AU - Sener, Melih

AU - Kleinekathöfer, Ulrich

AU - Vant, John W.

AU - Nguyen, Jonathan

AU - Hitchcock, Andrew

AU - Isralewitz, Barry

AU - Teo, Ivan

AU - Chandler, Danielle E.

AU - Stone, John E.

AU - Phillips, James C.

AU - Pogorelov, Taras V.

AU - Mallus, M. Ilaria

AU - Chipot, Christophe

AU - Luthey-Schulten, Zaida

AU - Tieleman, D. Peter

AU - Hunter, C. Neil

AU - Tajkhorshid, Emad

AU - Aksimentiev, Aleksei

AU - Schulten, Klaus

PY - 2019/11/14

Y1 - 2019/11/14

N2 - A full atomic resolution model of an entire organelle, the photosynthetic chromatophore vesicle of a purple bacterium, is constructed and reveals how the photosynthetic apparatus is optimized for ATP production in low-light habitats.

AB - A full atomic resolution model of an entire organelle, the photosynthetic chromatophore vesicle of a purple bacterium, is constructed and reveals how the photosynthetic apparatus is optimized for ATP production in low-light habitats.

KW - MD

KW - bioenergetics

KW - biological membranes

KW - charge transport

KW - chromatophore

KW - integrative model

KW - mitochondria

KW - molecular dynamics simulation

KW - optical spectroscopy

KW - photosynthesis

UR - http://www.scopus.com/inward/record.url?scp=85074397366&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2019.10.021

DO - 10.1016/j.cell.2019.10.021

M3 - Article

C2 - 31730852

AN - SCOPUS:85074397366

SN - 0092-8674

VL - 179

SP - 1098-1111.e23

JO - Cell

JF - Cell

IS - 5

ER -

Atoms to Phenotypes: Molecular Design Principles of Cellular Energy Metabolism

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