Ion-dependent protein–surface interactions from intrinsic solvent response

Prelesnik, Jesse L.; Alberstein, Robert G.; Zhang, Shuai; Pyles, Harley; Baker, David; Pfaendtner, Jim; De Yoreo, James J.; Tezcan, F. Akif; Remsing, Richard C.; Mundy, Christopher J.

doi:10.1073/pnas.2025121118

Ion-dependent protein–surface interactions from intrinsic solvent response

Journal Article · Fri Jun 25 00:00:00 EDT 2021 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2025121118· OSTI ID:1798553

^[1]; ^[2]; ^[3]; Pyles, Harley ^[4]; ^[5]; ^[6]; De Yoreo, James J. ^[3]; ^[7]; Remsing, Richard C. ^[8]; ^[9]

Department of Chemistry, University of Washington, Seattle, WA 98195,
Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA 92093,
Physical Sciences Division, Physical and Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA 99354,, Materials Science and Engineering, University of Washington, Seattle, WA 98195,
Department of Biochemistry, University of Washington, Seattle, WA 98195,, Institute for Protein Design, University of Washington, Seattle, WA 98195,
Department of Biochemistry, University of Washington, Seattle, WA 98195,, Institute for Protein Design, University of Washington, Seattle, WA 98195,, HHMI, University of Washington, Seattle, WA 98195,
Department of Chemistry, University of Washington, Seattle, WA 98195,, Department of Chemical Engineering, University of Washington, Seattle, WA 98195,
Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA 92093,, Materials Science and Engineering, University of California, San Diego, La Jolla, CA 92093,
Department of Chemistry and Chemical Biology, Rutgers University, Piscataway, NJ 08854,
Department of Chemical Engineering, University of Washington, Seattle, WA 98195,, Chemical Physics Theory Team, Pacific Northwest National Laboratory, Richland, WA 99354

Significance

Hard–soft interfaces between inorganic surfaces and biomolecules promote self-assembly processes with broad implications in biogeochemistry, energy sciences, nanomedicine, and origins of life. Yet, detailed molecular-scale understanding of inorganic–biomolecule interactions and their dependence on solution conditions is missing. We present a theory for the initial stages of inorganic–biomolecule assembly based on the far-field response of water, using experimentally characterized interactions between muscovite surfaces and mica-binding proteins as model systems. Our work connects molecular details of the solution to assembly outcomes and suggests the initial driving forces for assembly are dominated by long-range, ion-specific interactions. The connections made between interfacial structure and long-range surface–biomolecule interactions provide insights toward a predictive understanding of biomolecular self-assembly on mineral surfaces.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-76RL01830; SC0019288

OSTI ID:: 1798553

Alternate ID(s):: OSTI ID: 1810291
OSTI ID: 1821486

Report Number(s):: PNNL-SA--158527; e2025121118

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: 26 Vol. 118; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Engineering Biomolecular Self‐Assembly at Solid–Liquid Interfaces Zhang, Shuai; Chen, Jiajun; Liu, Jianli Advanced Materials, Vol. 33, Issue 23 https://doi.org/10.1002/adma.201905784	journal	July 2020
Biomineralization as an Inspiration for Materials Chemistry Nudelman, Fabio; Sommerdijk, Nico A. J. M. Angewandte Chemie International Edition, Vol. 51, Issue 27 https://doi.org/10.1002/anie.201106715	journal	May 2012
CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data Huang, Jing; MacKerell, Alexander D. Journal of Computational Chemistry, Vol. 34, Issue 25 https://doi.org/10.1002/jcc.23354	journal	July 2013
More bang for your buck: Improved use of GPU nodes for GROMACS 2018 Kutzner, Carsten; Páll, Szilárd; Fechner, Martin Journal of Computational Chemistry, Vol. 40, Issue 27 https://doi.org/10.1002/jcc.26011	journal	July 2019
Repulsion of interfaces due to boundary water Marčelja, S.; Radić, N. Chemical Physics Letters, Vol. 42, Issue 1 https://doi.org/10.1016/0009-2614(76)80567-2	journal	August 1976
Molecular layering of water in thin films between mica surfaces and its relation to hydration forces Pashley, Richard M.; Israelachvili, Jacob N. Journal of Colloid and Interface Science, Vol. 101, Issue 2 https://doi.org/10.1016/0021-9797(84)90063-8	journal	October 1984
Hydration repulsion between membranes and polar surfaces: Simulation approaches versus continuum theories Kanduč, Matej; Schlaich, Alexander; Schneck, Emanuel Advances in Colloid and Interface Science, Vol. 208 https://doi.org/10.1016/j.cis.2014.02.001	journal	June 2014
The physics of protein self-assembly McManus, Jennifer J.; Charbonneau, Patrick; Zaccarelli, Emanuela Current Opinion in Colloid & Interface Science, Vol. 22 https://doi.org/10.1016/j.cocis.2016.02.011	journal	April 2016
Molecular dynamics simulations of the colloidal interaction between smectite clay nanoparticles in liquid water Shen, Xinyi; Bourg, Ian C. Journal of Colloid and Interface Science, Vol. 584 https://doi.org/10.1016/j.jcis.2020.10.029	journal	February 2021
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers Abraham, Mark James; Murtola, Teemu; Schulz, Roland SoftwareX, Vol. 1-2 https://doi.org/10.1016/j.softx.2015.06.001	journal	September 2015
Closing the Gap Between Modeling and Experiments in the Self-Assembly of Biomolecules at Interfaces and in Solution Sampath, Janani; Alamdari, Sarah; Pfaendtner, Jim Chemistry of Materials, Vol. 32, Issue 19 https://doi.org/10.1021/acs.chemmater.0c01891	journal	August 2020
Self-Assembly of Colloidal Nanocrystals: From Intricate Structures to Functional Materials Boles, Michael A.; Engel, Michael; Talapin, Dmitri V. Chemical Reviews, Vol. 116, Issue 18 https://doi.org/10.1021/acs.chemrev.6b00196	journal	August 2016
Protein Assembly: Versatile Approaches to Construct Highly Ordered Nanostructures Luo, Quan; Hou, Chunxi; Bai, Yushi Chemical Reviews, Vol. 116, Issue 22 https://doi.org/10.1021/acs.chemrev.6b00228	journal	September 2016
Biasing Smarter, Not Harder, by Partitioning Collective Variables into Families in Parallel Bias Metadynamics Prakash, Arushi; Fu, Christopher D.; Bonomi, Massimiliano Journal of Chemical Theory and Computation, Vol. 14, Issue 10 https://doi.org/10.1021/acs.jctc.8b00448	journal	August 2018
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
Quantifying the Molecular-Scale Aqueous Response to the Mica Surface Prakash, Arushi; Pfaendtner, Jim; Chun, Jaehun The Journal of Physical Chemistry C, Vol. 121, Issue 34 https://doi.org/10.1021/acs.jpcc.7b03229	journal	August 2017
Effect of Hydrophilicity and Interfacial Water Structure on Particle Attachment Kerisit, Sebastien N.; De Yoreo, James J. The Journal of Physical Chemistry C, Vol. 124, Issue 9 https://doi.org/10.1021/acs.jpcc.9b12053	journal	February 2020
Multivalent Surface Cations Enhance Heterogeneous Freezing of Water on Muscovite Mica Lata, Nurun Nahar; Zhou, Jiarun; Hamilton, Pearce The Journal of Physical Chemistry Letters, Vol. 11, Issue 20 https://doi.org/10.1021/acs.jpclett.0c02121	journal	September 2020
The Electrostatic Screening Length in Concentrated Electrolytes Increases with Concentration Smith, Alexander M.; Lee, Alpha A.; Perkin, Susan The Journal of Physical Chemistry Letters, Vol. 7, Issue 12 https://doi.org/10.1021/acs.jpclett.6b00867	journal	May 2016
Identification of Single Adsorbed Cations on Mica–Liquid Interfaces by 3D Force Microscopy Martin-Jimenez, Daniel; Garcia, Ricardo The Journal of Physical Chemistry Letters, Vol. 8, Issue 23 https://doi.org/10.1021/acs.jpclett.7b02671	journal	November 2017
Direct Quantification of Water Surface Charge by Phase-Sensitive Second Harmonic Spectroscopy Dalstein, Laetitia; Chiang, Kuo-Yang; Wen, Yu-Chieh The Journal of Physical Chemistry Letters, Vol. 10, Issue 17 https://doi.org/10.1021/acs.jpclett.9b02156	journal	August 2019
Phenomena Affecting Catalytic Reactions at Solid–Liquid Interfaces Sievers, Carsten; Noda, Yu; Qi, Long ACS Catalysis, Vol. 6, Issue 12 https://doi.org/10.1021/acscatal.6b02532	journal	November 2016
Atomic- and Molecular-Resolution Mapping of Solid–Liquid Interfaces by 3D Atomic Force Microscopy Fukuma, Takeshi; Garcia, Ricardo ACS Nano, Vol. 12, Issue 12 https://doi.org/10.1021/acsnano.8b07216	journal	November 2018
Metal-Directed Protein Self-Assembly Salgado, Eric N.; Radford, Robert J.; Tezcan, F. Akif Accounts of Chemical Research, Vol. 43, Issue 5 https://doi.org/10.1021/ar900273t	journal	May 2010
Use of Ion Exchange To Regulate the Heterogeneous Ice Nucleation Efficiency of Mica Jin, Shenglin; Liu, Yuan; Deiseroth, Malte Journal of the American Chemical Society, Vol. 142, Issue 42 https://doi.org/10.1021/jacs.0c00920	journal	September 2020
Molecular Models of Hydroxide, Oxyhydroxide, and Clay Phases and the Development of a General Force Field Cygan, Randall T.; Liang, Jian-Jie; Kalinichev, Andrey G. The Journal of Physical Chemistry B, Vol. 108, Issue 4 https://doi.org/10.1021/jp0363287	journal	January 2004
Hydrophobicity Scaling of Aqueous Interfaces by an Electrostatic Mapping Remsing, Richard C.; Weeks, John D. The Journal of Physical Chemistry B, Vol. 119, Issue 29 https://doi.org/10.1021/jp509903n	journal	September 2014
Determination of Alkali and Halide Monovalent Ion Parameters for Use in Explicitly Solvated Biomolecular Simulations Joung, In Suk; Cheatham, Thomas E. The Journal of Physical Chemistry B, Vol. 112, Issue 30 https://doi.org/10.1021/jp8001614	journal	July 2008
Epitaxially Guided Assembly of Collagen Layers on Mica Surfaces Leow, Wee Wen; Hwang, Wonmuk Langmuir, Vol. 27, Issue 17 https://doi.org/10.1021/la2018055	journal	September 2011
Thermodynamically Consistent Force Fields for the Assembly of Inorganic, Organic, and Biological Nanostructures: The INTERFACE Force Field Heinz, Hendrik; Lin, Tzu-Jen; Kishore Mishra, Ratan Langmuir, Vol. 29, Issue 6 https://doi.org/10.1021/la3038846	journal	January 2013
Potassium Ion Mediated Collagen Microfibril Assembly on Mica Loo, Richard W.; Goh, M. Cynthia Langmuir, Vol. 24, Issue 23 https://doi.org/10.1021/la803041v	journal	December 2008
Heteroepitaxial Streptavidin Nanocrystals Reveal Critical Role of Proton “Fingers” and Subsurface Atoms in Determining Adsorbed Protein Orientation Czajkowsky, Daniel M.; Li, Lin; Sun, Jielin ACS Nano, Vol. 6, Issue 1 https://doi.org/10.1021/nn203356p	journal	December 2011
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
Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals Suzuki, Yuta; Cardone, Giovanni; Restrepo, David Nature, Vol. 533, Issue 7603 https://doi.org/10.1038/nature17633	journal	May 2016
Atomically resolved three-dimensional structures of electrolyte aqueous solutions near a solid surface Martin-Jimenez, Daniel; Chacon, Enrique; Tarazona, Pedro Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12164	journal	July 2016
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
Direction-specific interaction forces underlying zinc oxide crystal growth by oriented attachment Zhang, X.; Shen, Z.; Liu, J. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00844-6	journal	October 2017
Connecting energetics to dynamics in particle growth by oriented attachment using real-time observations Liu, Lili; Nakouzi, Elias; Sushko, Maria L. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14719-w	journal	February 2020
Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions Zhang, Shuai; Alberstein, Robert G.; De Yoreo, James J. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17562-1	journal	July 2020
Engineering the entropy-driven free-energy landscape of a dynamic nanoporous protein assembly Alberstein, Robert; Suzuki, Yuta; Paesani, Francesco Nature Chemistry, Vol. 10, Issue 7 https://doi.org/10.1038/s41557-018-0053-4	journal	April 2018
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
Direct observation of the dynamics of single metal ions at the interface with solids in aqueous solutions Ricci, Maria; Trewby, William; Cafolla, Clodomiro Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43234	journal	February 2017
The origin of facet selectivity and alignment in anatase TiO ₂ nanoparticles in electrolyte solutions: implications for oriented attachment in metal oxides Sushko, M. L.; Rosso, K. M. Nanoscale, Vol. 8, Issue 47 https://doi.org/10.1039/C6NR06953C	journal	January 2016
New tricks for old dogs: improving the accuracy of biomolecular force fields by pair-specific corrections to non-bonded interactions Yoo, Jejoong; Aksimentiev, Aleksei Physical Chemistry Chemical Physics, Vol. 20, Issue 13 https://doi.org/10.1039/C7CP08185E	journal	January 2018
Electromechanics of the liquid water vapour interface Zhang, Chao; Sprik, Michiel Physical Chemistry Chemical Physics, Vol. 22, Issue 19 https://doi.org/10.1039/C9CP06901A	journal	January 2020
Local molecular field theory for effective attractions between like charged objects in systems with strong Coulomb interactions Chen, Y. -G.; Weeks, J. D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 20 https://doi.org/10.1073/pnas.0600282103	journal	May 2006
Long-ranged contributions to solvation free energies from theory and short-ranged models Remsing, Richard C.; Liu, Shule; Weeks, John D. Proceedings of the National Academy of Sciences, Vol. 113, Issue 11 https://doi.org/10.1073/pnas.1521570113	journal	February 2016
Trends in mica–mica adhesion reflect the influence of molecular details on long-range dispersion forces underlying aggregation and coalignment Li, Dongsheng; Chun, Jaehun; Xiao, Dongdong Proceedings of the National Academy of Sciences, Vol. 114, Issue 29 https://doi.org/10.1073/pnas.1621186114	journal	July 2017
The effects of deviations from Lorentz–Berthelot rules on the properties of a simple mixture Boda, Dezső; Henderson, Douglas Molecular Physics, Vol. 106, Issue 20 https://doi.org/10.1080/00268970802471137	journal	October 2008
On the efficient and accurate short-ranged simulations of uniform polar molecular liquids Rodgers, Jocelyn M.; Hu, Zhonghan; Weeks, John D. Molecular Physics, Vol. 109, Issue 7-10 https://doi.org/10.1080/00268976.2011.554332	journal	March 2011
Local molecular field theory for the treatment of electrostatics Rodgers, Jocelyn M.; Weeks, John D. Journal of Physics: Condensed Matter, Vol. 20, Issue 49 https://doi.org/10.1088/0953-8984/20/49/494206	journal	November 2008
Mineral Surfaces, Geochemical Complexities, and the Origins of Life Hazen, R. M.; Sverjensky, D. A. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 5 https://doi.org/10.1101/cshperspect.a002162	journal	April 2010
Interface-sensitive imaging by an image reconstruction aided X-ray reflectivity technique Jiang, Jinxing; Hirano, Keiichi; Sakurai, Kenji Journal of Applied Crystallography, Vol. 50, Issue 3 https://doi.org/10.1107/S160057671700509X	journal	May 2017
Direction-Specific Interactions Control Crystal Growth by Oriented Attachment Li, D.; Nielsen, M. H.; Lee, J. R. I. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1219643	journal	May 2012
Alzheimer's and Parkinson's diseases: The prion concept in relation to assembled A , tau, and -synuclein Goedert, M. Science, Vol. 349, Issue 6248 https://doi.org/10.1126/science.1255555	journal	August 2015
Before enzymes and templates: theory of surface metabolism Wächtershäuser, G. Microbiological Reviews, Vol. 52, Issue 4 https://doi.org/10.1128/mr.52.4.452-484.1988	journal	December 1988
C ONNECTING L OCAL S TRUCTURE TO I NTERFACE F ORMATION : A Molecular Scale van der Waals Theory of Nonuniform Liquids Weeks, John D. Annual Review of Physical Chemistry, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.physchem.53.100201.133929	journal	October 2002
Thermodynamics at Solid–Liquid Interfaces Frank, Michael; Drikakis, Dimitris Entropy, Vol. 20, Issue 5 https://doi.org/10.3390/e20050362	journal	May 2018
Biomineralization Forming Process and Bio-inspired Nanomaterials for Biomedical Application: A Review Chen, Yuanyuan; Feng, Yanmin; Deveaux, John Gregory Minerals, Vol. 9, Issue 2 https://doi.org/10.3390/min9020068	journal	January 2019

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