Large-Scale Molecular Dynamics Simulations of Cellular Compartments.

Ensemble toolkit High-performance computing Molecular dynamics Multiscale simulation NAMD Photosynthetic chromatophore VMD

Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2021
Historique:
entrez: 20 4 2021
pubmed: 21 4 2021
medline: 12 8 2021
Statut: ppublish

Résumé

Molecular dynamics or MD simulation is gradually maturing into a tool for constructing in vivo models of living cells in atomistic details. The feasibility of such models is bolstered by integrating the simulations with data from microscopic, tomographic and spectroscopic experiments on exascale supercomputers, facilitated by the use of deep learning technologies. Over time, MD simulation has evolved from tens of thousands of atoms to over 100 million atoms comprising an entire cell organelle, a photosynthetic chromatophore vesicle from a purple bacterium. In this chapter, we present a step-by-step outline for preparing, executing and analyzing such large-scale MD simulations of biological systems that are essential to life processes. All scripts are provided via GitHub.

Identifiants

pubmed: 33877636
doi: 10.1007/978-1-0716-1394-8_18
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

335-356

Subventions

Organisme : NIGMS NIH HHS
ID : P41 GM104601
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM098243
Pays : United States

Références

Alberts B (2010) Cell biology: the endless frontier. Mol Biol Cell 21(22):3785
pubmed: 21079009 pmcid: 2982093 doi: 10.1091/mbc.e10-04-0334
Singharoy A, Maffeo C, Delgado-Magnero K et al (2019) Atoms to phenotypes: molecular design principles of cellular energy metabolism. Cell 179(5):1098–1111.e23
pubmed: 31730852 pmcid: 7075482 doi: 10.1016/j.cell.2019.10.021
Goh BC, Hadden JA, Bernardi RC et al (2016) Computational methodologies for real-space structural refinement of large macromolecular complexes. Annu Rev Biophys 45:253–278
pubmed: 27145875 pmcid: 5526348 doi: 10.1146/annurev-biophys-062215-011113
Voth GA (2017) A multiscale description of biomolecular active matter: the chemistry underlying many life processes. Acc Chem Res 50(3):594–598
pubmed: 28945406 doi: 10.1021/acs.accounts.6b00572
Davtyan A, Simunovic M, Voth GA (2016) Multiscale simulations of protein-facilitated membrane remodeling. J Struct Biol 196(1):57–63
pubmed: 27327264 pmcid: 5031523 doi: 10.1016/j.jsb.2016.06.012
Van Meel JA, Arnold A, Frenkel D et al (2008) Harvesting graphics power for md simulations. Mol Simul 34(3):259–266
doi: 10.1080/08927020701744295
Ananthraj V, De K, Jha S et al (2018) Towards exascale computing for high energy physics: The atlas experience at ornl. In: 2018 IEEE 14th international conference on e-science (e-science), pp 341–342
doi: 10.1109/eScience.2018.00086
Kilburg D, Gallicchio E (2016) Recent advances in computational models for the study of protein–peptide interactions. Adv Protein Chem Struct Biol 105:27–57
pubmed: 27567483 doi: 10.1016/bs.apcsb.2016.06.002
Ourmazd A (2019) Cryo-em, xfels and the structure conundrum in structural biology. Nat Methods 16(10):941–944
pubmed: 31534229 doi: 10.1038/s41592-019-0587-4
Marrink SJ, Corradi V, Souza PC et al (2019) Computational modeling of realistic cell membranes. Chem Rev 119(9):6184–6226
pubmed: 30623647 pmcid: 6509646 doi: 10.1021/acs.chemrev.8b00460
Feig M, Harada R, Mori T et al (2015) Complete atomistic model of a bacterial cytoplasm for integrating physics, biochemistry, and systems biology. J Mol Graph Model 58:1–9
pubmed: 25765281 pmcid: 4388805 doi: 10.1016/j.jmgm.2015.02.004
Yu I, Mori T, Ando T et al (2016) Biomolecular interactions modulate macromolecular structure and dynamics in atomistic model of a bacterial cytoplasm. elife 5:e19274
pubmed: 27801646 pmcid: 5089862 doi: 10.7554/eLife.19274
Perilla JR, Schulten K (2017) Physical properties of the hiv-1 capsid from all-atom molecular dynamics simulations. Nat Commun 8:15959
pubmed: 28722007 pmcid: 5524983 doi: 10.1038/ncomms15959
Wickles S, Singharoy A, Andreani J et al (2014) A structural model of the active ribosome-bound membrane protein insertase yidc. elife 3:e03035
pubmed: 25012291 pmcid: 4124156 doi: 10.7554/eLife.03035
Trabuco LG, Villa E, Mitra K et al (2008) Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16(5):673–683
pubmed: 18462672 pmcid: 2430731 doi: 10.1016/j.str.2008.03.005
Schweitzer A, Aufderheide A, al Rudack T (2016) Structure of the human 26s proteasome at a resolution of 3.9 Å. Proc Natl Acad Sci U S A 113(28):7816–7821
pubmed: 27342858 pmcid: 4948313 doi: 10.1073/pnas.1608050113
Durrant JD, Bush RM, Amaro RE (2016) Microsecond molecular dynamics simulations of influenza neuraminidase suggest a mechanism for the increased virulence of stalk-deletion mutants. J Phys Chem B 120(33):8590–8599
pubmed: 27141956 pmcid: 5002936 doi: 10.1021/acs.jpcb.6b02655
Mannige RV, Brooks CL III (2010) Periodic table of virus capsids: implications for natural selection and design. PLoS One 5(3):e9423
pubmed: 20209096 pmcid: 2831995 doi: 10.1371/journal.pone.0009423
Blood PD, Voth GA (2006) Direct observation of bin/amphiphysin/rvs (bar) domaininduced membrane curvature by means of molecular dynamics simulations. Proc Natl Acad Sci U S A 103(41):15068–15072
pubmed: 17008407 pmcid: 1622778 doi: 10.1073/pnas.0603917103
Arkhipov A, Yin Y, Schulten K (2008) Four-scale description of membrane sculpting by bar domains. Biophys J 95(6):2806–2821
pubmed: 18515394 pmcid: 2527247 doi: 10.1529/biophysj.108.132563
Jung J, Nishima W, Daniels M et al (2019) Scaling molecular dynamics beyond 100,000 processor cores for large-scale biophysical simulations. J Comput Chem 40(21):1919–1930
pubmed: 30994934 pmcid: 7153361 doi: 10.1002/jcc.25840
Renaud J-P, Chari A, Ciferri C et al (2018) Cryo-EM in drug discovery: achievements, limitations and prospects. Nat Rev Drug Discov 17(7):471–492
pubmed: 29880918 doi: 10.1038/nrd.2018.77
Camargo C (2018) Physics makes rules, evolution rolls the dice. Science 361(6399):236–236
doi: 10.1126/science.aat7776
Şener MK, Olsen JD, Hunter CN et al (2007) Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. Proc Natl Acad Sci 104(40):15723–15728
pubmed: 17895378 doi: 10.1073/pnas.0706861104
Blankenship RE (2014) Molecular mechanisms of photosynthesis. John Wiley & Sons, Hoboken, New Jersey
Vant, J. W. (2019). Chromatophore_large_system_simulation. https://github.com/jvant/Chromatophore_Large_System_Simulation GitHub
Phillips JC, Braun R, Wang W et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16):1781–1802
pubmed: 16222654 pmcid: 2486339 doi: 10.1002/jcc.20289
Comer J, Aksimentiev A (2016) DNA sequence-dependent ionic currents in ultra-small solidstate nanopores. Nanoscale 8(18):9600–9613
pubmed: 27103233 pmcid: 4860951 doi: 10.1039/C6NR01061J
Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14(1):33–38
pubmed: 8744570 doi: 10.1016/0263-7855(96)00018-5 pmcid: 8744570
Singharoy A, Cheluvaraja S, Ortoleva P (2011) Order parameters for macromolecules: application to multiscale simulation. J Chem Phys 134(4):044104
pubmed: 21280684 pmcid: 3045216 doi: 10.1063/1.3524532
Acun B, Hardy DJ, Kale LV et al (2018) Scalable molecular dynamics with NAMD on the summit system. IBM J Res Dev 62(6):1–9
pubmed: 32154805 doi: 10.1147/JRD.2018.2888986
Chandler DE, Strümpfer J, Sener M et al (2014) Light harvesting by lamellar chromatophores in rhodospirillum photometricum. Biophys J 106(11):2503–2510
pubmed: 24896130 pmcid: 4052275 doi: 10.1016/j.bpj.2014.04.030
Şener M, Strümpfer J, Timney JA et al (2010) Photosynthetic vesicle architecture and constraints on efficient energy and harvesting. Biophys J 99(1):67–75
pubmed: 20655834 pmcid: 2895385 doi: 10.1016/j.bpj.2010.04.013
Cartron ML, Olsen JD, Sener M et al (2014) Integration of energy and electron transfer processes in the photosynthetic membrane of rhodobacter sphaeroides. Biochim Biophys Acta 1837(10):1769–1780
pubmed: 24530865 pmcid: 4143486 doi: 10.1016/j.bbabio.2014.02.003
Kumar S, Cartron ML, Mullin N et al (2016) Direct imaging of protein organization in an intact bacterial organelle using high-resolution atomic force microscopy. ACS Nano 11(1):126–133
pubmed: 28114766 pmcid: 5269641 doi: 10.1021/acsnano.6b05647
Scheuring S, Nevo R, Liu L-N et al (2014) The architecture of rhodobacter sphaeroides chromatophores. Biochim Biophys Acta 1837(8):1263–1270
pubmed: 24685429 doi: 10.1016/j.bbabio.2014.03.011
Russel D, Lasker K, Webb B et al (2012) Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies. PLoS Biol 10(1):e1001244
pubmed: 22272186 pmcid: 3260315 doi: 10.1371/journal.pbio.1001244
Ho PT, Montiel-Garcia DJ, Wong JJ et al (2018) VIPERdb: a tool for virus research. Annu Rev Virol 5(1):477–488
pubmed: 30265627 doi: 10.1146/annurev-virology-092917-043405
Durrant JD, Amaro RE (2014) Lipidwrapper: an algorithm for generating large-scale membrane models of arbitrary geometry. PLoS Comput Biol 10(7):e1003720
pubmed: 25032790 pmcid: 4102414 doi: 10.1371/journal.pcbi.1003720
Wells DB, Abramkina V, Aksimentiev A (2007) Exploring transmembrane transport through α-hemolysin with grid-steered molecular dynamics. J Chem Phys 127(12):09B619
doi: 10.1063/1.2770738
Balasubramanian V, Turilli M, Hu W et al (2018) Harnessing the power of many: extensible toolkit for scalable ensemble applications. In: In 2018 IEEE international parallel and distributed processing symposium (ipdps). IEEE, New York, pp 536–545
doi: 10.1109/IPDPS.2018.00063
Turilli M, Santcroos M, Jha S (2018) A comprehensive perspective on pilot-job systems. ACM Comput Surv 51(2):43:1–43:32
doi: 10.1145/3177851
Goodale T, Jha S, Kaiser H et al (2006) SAGA: a simple API for grid applications, high-level application programming on the grid. Comput Methods Sci Technol 12(1):7–20
doi: 10.12921/cmst.2006.12.01.07-20
Merzky A, Weidner O, Jha S (2015) SAGA: a standardized access layer to heterogeneous distributed computing infrastructure. Software-X 1-2:3–8
MDFF Integration with EnTK on OLCF Summit. (2019). https://github.com/radical-collaboration/MDFF-Error.GitHub
Chandler DE, Hsin J, Harrison CB et al (2008) Intrinsic curvature properties of photosynthetic proteins in chromatophores. Biophys J 95(6):2822–2836
pubmed: 18515401 pmcid: 2527265 doi: 10.1529/biophysj.108.132852
Singharoy A, Barragan AM, Thangapandian S et al (2016b) Binding site recognition and docking dynamics of a single electron transport protein: cytochrome c 2. J Am Chem Soc 138(37):12077–12089
pubmed: 27508459 pmcid: 5518707 doi: 10.1021/jacs.6b01193
Singharoy A, Teo I, McGreevy R et al (2016a) Molecular dynamics-based model refinement and validation for sub-5 angstrom cryo-electron microscopy maps. eLife 5:e16105
pubmed: 27383269 pmcid: 4990421 doi: 10.7554/eLife.16105

Auteurs

Eric Wilson (E)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA.

John Vant (J)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA.

Jacob Layton (J)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA.

Ryan Boyd (R)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA.

Hyungro Lee (H)

RADICAL, ECE, Rutgers University, Piscataway, NJ, USA.

Matteo Turilli (M)

RADICAL, ECE, Rutgers University, Piscataway, NJ, USA.

Benjamín Hernández (B)

Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Sean Wilkinson (S)

Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Shantenu Jha (S)

RADICAL, ECE, Rutgers University, Piscataway, NJ, USA.
Brookhaven National Laboratory, Upton, NY, USA.

Chitrak Gupta (C)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA. cgupta11@asu.edu.

Daipayan Sarkar (D)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA. dsarkar@asu.edu.
Department of Biological Sciences, Purdue University, West Lafayette, IN, USA. dsarkar@asu.edu.

Abhishek Singharoy (A)

The School of Molecular Sciences, Arizona State University, Tempe, AZ, USA. asinghar@asu.edu.

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