Rotational dynamics and transition mechanisms of surface-adsorbed proteins

Zhang, Shuai; Sadre, Robbie; Legg, Benjamin A.; Pyles, Harley; Perciano, Talita; Bethel, E. Wes; Baker, David; Rübel, Oliver; De Yoreo, James J.

doi:10.1073/pnas.2020242119

Rotational dynamics and transition mechanisms of surface-adsorbed proteins

Journal Article · Mon Apr 11 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2020242119· OSTI ID:1865688

^[1]; Sadre, Robbie ^[2]; Legg, Benjamin A. ^[3]; Pyles, Harley ^[4]; ^[2]; ^[5]; ^[4]; Rübel, Oliver ^[2]; De Yoreo, James J. ^[3]

Univ. of Washington, Seattle, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Pacific Northwest National Laboratory
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Washington, Seattle, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Univ. of Washington, Seattle, WA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); San Francisco State Univ., CA (United States)

The exquisite organization exhibited by hybrid biomolecular–inorganic materials in nature has inspired the development of synthetic analogues for numerous applications. Nevertheless, a mechanistic picture of the energetic controls and response dynamics leading to organization is lacking. Furthermore, we pair high-speed atomic force microscopy with machine learning and Monte Carlo simulations to analyze the rotational dynamics of rod-like proteins on a crystal lattice, simultaneously quantifying the orientational energy landscape and transition probabilities between energetically favorable orientations. Although rotations largely follow Brownian diffusion, proteins often make large jumps in orientation, thus rapidly overcoming barriers that usually inhibit rotation. Moreover, the rotational dynamics can be tuned via protein size and solution chemistry, providing tools for controlling biomolecular assembly at inorganic interfaces.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Univ. of Washington, Seattle, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Advanced Scientific Computing Research (ASCR); USDOE Office of Science (SC), Advanced Scientific Computing Research (ASCR). Scientific Discovery through Advanced Computing (SciDAC); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0019288

OSTI ID:: 1865688

Alternate ID(s):: OSTI ID: 1864715
OSTI ID: 1893118

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 16 Vol. 119; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (40)

Software for drift compensation, particle tracking and particle analysis of high-speed atomic force microscopy image series: SOFTWARE FOR HIGH-SPEED ATOMIC FORCE MICROSCOPY IMAGE SERIES Husain, Mohamed; Boudier, Thomas; Paul-Gilloteaux, Perrine Journal of Molecular Recognition, Vol. 25, Issue 5 https://doi.org/10.1002/jmr.2187	journal	April 2012
U-Net: Convolutional Networks for Biomedical Image Segmentation Ronneberger, Olaf; Fischer, Philipp; Brox, Thomas Medical Image Computing and Computer-Assisted Intervention – MICCAI 2015: 18th International Conference, Munich, Germany, October 5-9, 2015, Proceedings, Part III https://doi.org/10.1007/978-3-319-24574-4_28	book	November 2015
Hydration forces between mica surfaces in aqueous electrolyte solutions Pashley, R. M. Journal of Colloid and Interface Science, Vol. 80, Issue 1 https://doi.org/10.1016/0021-9797(81)90171-5	journal	March 1981
Contrast Limited Adaptive Histogram Equalization Zuiderveld, Karel Graphics Gems https://doi.org/10.1016/B978-0-12-336156-1.50061-6	book	January 1994
Radio frequency interference mitigation using deep convolutional neural networks Akeret, J.; Chang, C.; Lucchi, A. Astronomy and Computing, Vol. 18 https://doi.org/10.1016/j.ascom.2017.01.002	journal	January 2017
Tackling the Challenges of Dynamic Experiments Using Liquid-Cell Transmission Electron Microscopy Parent, Lucas R.; Bakalis, Evangelos; Proetto, Maria Accounts of Chemical Research, Vol. 51, Issue 1 https://doi.org/10.1021/acs.accounts.7b00331	journal	December 2017
Desorption-Mediated Motion of Nanoparticles at the Liquid–Solid Interface Chee, See Wee; Baraissov, Zhaslan; Loh, N. Duane The Journal of Physical Chemistry C, Vol. 120, Issue 36 https://doi.org/10.1021/acs.jpcc.6b07983	journal	September 2016
Stern Layer Structure and Energetics at Mica–Water Interfaces Bourg, Ian C.; Lee, Sang Soo; Fenter, Paul The Journal of Physical Chemistry C, Vol. 121, Issue 17 https://doi.org/10.1021/acs.jpcc.7b01828	journal	April 2017
Direct Observations of the Rotation and Translation of Anisotropic Nanoparticles Adsorbed at a Liquid–Solid Interface Chee, See Wee; Anand, Utkarsh; Bisht, Geeta Nano Letters, Vol. 19, Issue 5 https://doi.org/10.1021/acs.nanolett.8b04962	journal	March 2019
Big, Deep, and Smart Data in Scanning Probe Microscopy Kalinin, Sergei V.; Strelcov, Evgheni; Belianinov, Alex ACS Nano, Vol. 10, Issue 10 https://doi.org/10.1021/acsnano.6b04212	journal	September 2016
Recursive Directional Ligation by Plasmid Reconstruction Allows Rapid and Seamless Cloning of Oligomeric Genes McDaniel, Jonathan R.; MacKay, J. Andrew; Quiroz, Felipe García Biomacromolecules, Vol. 11, Issue 4 https://doi.org/10.1021/bm901387t	journal	April 2010
Filming Biomolecular Processes by High-Speed Atomic Force Microscopy Ando, Toshio; Uchihashi, Takayuki; Scheuring, Simon Chemical Reviews, Vol. 114, Issue 6 https://doi.org/10.1021/cr4003837	journal	January 2014
Supramolecular Nanopatterns Self-Assembled by Adenine−Thymine Quartets at the Liquid/Solid Interface Mamdouh, Wael; Dong, Mingdong; Xu, Sailong Journal of the American Chemical Society, Vol. 128, Issue 40 https://doi.org/10.1021/ja064988u	journal	September 2006
Single-Molecule Tracking of Polymer Surface Diffusion Skaug, Michael J.; Mabry, Joshua N.; Schwartz, Daniel K. Journal of the American Chemical Society, Vol. 136, Issue 4 https://doi.org/10.1021/ja407396v	journal	November 2013
Nanocrystal Diffusion in a Liquid Thin Film Observed by in Situ Transmission Electron Microscopy Zheng, Haimei; Claridge, Shelley A.; Minor, Andrew M. Nano Letters, Vol. 9, Issue 6 https://doi.org/10.1021/nl9012369	journal	June 2009
Exploring the repeat protein universe through computational protein design Brunette, Tj; Parmeggiani, Fabio; Huang, Po-Ssu Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16162	journal	December 2015
Water-induced correlation between single ions imaged at the solid–liquid interface Ricci, Maria; Spijker, Peter; Voïtchovsky, Kislon Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5400	journal	July 2014
Self-assembly of two-dimensional DNA origami lattices using cation-controlled surface diffusion Woo, Sungwook; Rothemund, Paul W. K. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5889	journal	September 2014
Observing classical nucleation theory at work by monitoring phase transitions with molecular precision Sleutel, Mike; Lutsko, Jim; Van Driessche, Alexander E. S. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6598	journal	December 2014
The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors Nudelman, Fabio; Pieterse, Koen; George, Anne Nature Materials, Vol. 9, Issue 12 https://doi.org/10.1038/nmat2875	journal	October 2010
When Brownian diffusion is not Gaussian Wang, Bo; Kuo, James; Bae, Sung Chul Nature Materials, Vol. 11, Issue 6 https://doi.org/10.1038/nmat3308	journal	May 2012
Immunoactive two-dimensional self-assembly of monoclonal antibodies in aqueous solution revealed by atomic force microscopy Ido, Shinichiro; Kimiya, Hirokazu; Kobayashi, Kei Nature Materials, Vol. 13, Issue 3 https://doi.org/10.1038/nmat3847	journal	January 2014
Molecular biomimetics: nanotechnology through biology Sarikaya, Mehmet; Tamerler, Candan; Jen, Alex K. -Y. Nature Materials, Vol. 2, Issue 9 https://doi.org/10.1038/nmat964	journal	September 2003
Protein-based organelles in bacteria: carboxysomes and related microcompartments Yeates, Todd O.; Kerfeld, Cheryl A.; Heinhorst, Sabine Nature Reviews Microbiology, Vol. 6, Issue 9 https://doi.org/10.1038/nrmicro1913	journal	August 2008
Distribution, formation and regulation of gas vesicles Pfeifer, Felicitas Nature Reviews Microbiology, Vol. 10, Issue 10 https://doi.org/10.1038/nrmicro2834	journal	September 2012
Controlling protein assembly on inorganic crystals through designed protein interfaces Pyles, Harley; Zhang, Shuai; De Yoreo, James J. Nature, Vol. 571, Issue 7764 https://doi.org/10.1038/s41586-019-1361-6	journal	July 2019
Hierarchical construction of self-assembled low-dimensional molecular architectures observed by using scanning tunneling microscopy Yang, Yanlian; Wang, Chen Chemical Society Reviews, Vol. 38, Issue 9 https://doi.org/10.1039/b807500j	journal	January 2009
Direct observation of kinetic traps associated with structural transformations leading to multiple pathways of S-layer assembly Shin, S. -H.; Chung, S.; Sanii, B. Proceedings of the National Academy of Sciences, Vol. 109, Issue 32 https://doi.org/10.1073/pnas.1201504109	journal	July 2012
S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays Moll, D.; Huber, C.; Schlegel, B. Proceedings of the National Academy of Sciences, Vol. 99, Issue 23 https://doi.org/10.1073/pnas.232299399	journal	November 2002
Intermittent Molecular Hopping at the Solid-Liquid Interface Skaug, Michael J.; Mabry, Joshua; Schwartz, Daniel K. Physical Review Letters, Vol. 110, Issue 25 https://doi.org/10.1103/PhysRevLett.110.256101	journal	June 2013
Thermodynamics of Anomalous Diffusion Zanette, Damián H.; Alemany, Pablo A. Physical Review Letters, Vol. 75, Issue 3 https://doi.org/10.1103/PhysRevLett.75.366	journal	July 1995
The structure of muscovite, KAl ₂ (Si ₃ Al)O ₁₀ (OH) ₂ Radoslovich, E. W. Acta Crystallographica, Vol. 13, Issue 11 https://doi.org/10.1107/S0365110X60002259	journal	November 1960
The Fractal Geometry of Nature Mandelbrot, Benoit B.; Wheeler, John A. American Journal of Physics, Vol. 51, Issue 3 https://doi.org/10.1119/1.13295	journal	March 1983
Protein Structures Forming the Shell of Primitive Bacterial Organelles Kerfeld, C. A. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1113397	journal	August 2005
Molecular Recognition at Crystal Interfaces Weissbuch, I.; Addadi, L.; Leiserowitz, L. Science, Vol. 253, Issue 5020 https://doi.org/10.1126/science.253.5020.637	journal	August 1991
Macromolecular recognition directs calcium ions to coccolith mineralization sites Gal, Assaf; Wirth, Richard; Kopka, Joachim Science, Vol. 353, Issue 6299 https://doi.org/10.1126/science.aaf7889	journal	August 2016
Building two-dimensional materials one row at a time: Avoiding the nucleation barrier Chen, Jiajun; Zhu, Enbo; Liu, Juan Science, Vol. 362, Issue 6419 https://doi.org/10.1126/science.aau4146	journal	December 2018
Molecular Chaperone Functions in Protein Folding and Proteostasis Kim, Yujin E.; Hipp, Mark S.; Bracher, Andreas Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-060208-092442	journal	June 2013
Principles of Crystal Nucleation and Growth De Yoreo, J. J. Reviews in Mineralogy and Geochemistry, Vol. 54, Issue 1 https://doi.org/10.2113/0540057	journal	January 2003
Adolf Fick and Diffusion Equations Philibert, Jean Defect and Diffusion Forum, Vol. 249 https://doi.org/10.4028/www.scientific.net/DDF.249.1	journal	January 2006

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