The Anisotropic Adsorption of De Novo Allosteric Two‐Component Protein Fibers on Mica Surfaces

Shi, Chenyang; Shen, Hao; Bae, Yuna; Heo, Jaeyoung; Zhang, Shuai; Yao, Lehan; Baker, David; De Yoreo, James J.

doi:10.1002/adfm.202520864

The Anisotropic Adsorption of De Novo Allosteric Two‐Component Protein Fibers on Mica Surfaces

Journal Article · Tue Nov 11 00:00:00 EST 2025 · Advanced Functional Materials

DOI:https://doi.org/10.1002/adfm.202520864· OSTI ID:3003728

Shi, Chenyang ^[1]; Shen, Hao ^[2]; Bae, Yuna ^[1]; Heo, Jaeyoung ^[1]; Zhang, Shuai ^[3]; Yao, Lehan ^[1]; Baker, David ^[2]; ^[3]

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

Protein adsorption at solid–liquid interfaces underlies many biomedical and materials applications, yet the mechanisms governing adsorption of proteins and their assemblies remain poorly understood. Here we investigate de novo–designed proteins that self-assemble into three fibrillar morphologies — small (S), large (L), and helical (H)—on muscovite mica. S-fibers are metastable, forming first but diminishing as L- and H-fibers develop and deposit. Adsorption of both fibers and monomers depends on fiber morphology and solvent environment, which is modulated by the substrate. The anisotropic surface features of the fiber types—long axis of S- and L-fibers and helical grooves of H-fibers—correlate with specific crystallographic directions on mica (001). S- and L-fibers align along the unique lattice axis, while the substrate-facing groove of H-fibers preferentially aligns along the remaining symmetry-related directions. Increasing potassium chloride (KCl) concentrations to molar levels alters adsorption, decreasing monomer coverage relative to fibers. These observations, interpreted through the effect of interfacial interface, indicate that ion-mediated modulation of hydration layers governs electrostatic interactions and alignment. This study reveals how coupling between protein topography, substrate crystallography, and hydration structure dictates selective adsorption and orientation of protein assemblies, offering insights for rational biomolecular material design.

View Accepted Manuscript (DOE)

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:: 3003728

Journal Information:: Advanced Functional Materials, Journal Name: Advanced Functional Materials; ISSN 1616-301X; ISSN 1616-3028

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (52)

Controlling Protein Adsorption through Nanostructured Polymeric Surfaces Firkowska-Boden, Izabela; Zhang, Xiaoyuan; Jandt, Klaus D. Advanced Healthcare Materials, Vol. 7, Issue 1 https://doi.org/10.1002/adhm.201700995	journal	November 2017
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
Manipulating the Assembly and Architecture of Fibrillar Silk Shi, Chenyang; Bae, Yuna; Zhang, Mingyi Advanced Materials, Vol. 37, Issue 24 https://doi.org/10.1002/adma.202501096	journal	April 2025
Unveiling the nanoscale architectures and dynamics of protein assembly with in situ atomic force microscopy Zhai, Zhaoyi; Schmid, Sakshi Yadav; Lin, Zhixing Aggregate, Vol. 5, Issue 5 https://doi.org/10.1002/agt2.604	journal	May 2024
Mechanisms of Biomolecular Self‐Assembly Investigated Through In Situ Observations of Structures and Dynamics Schmid, Sakshi Yadav; Lachowski, Kacper; Chiang, Huat Thart Angewandte Chemie International Edition, Vol. 62, Issue 48 https://doi.org/10.1002/anie.202309725	journal	September 2023
Protein Needles Designed to Self‐Assemble through Needle Tip Engineering Kikuchi, Kosuke; Fukuyama, Tatsuya; Uchihashi, Takayuki Small, Vol. 18, Issue 10 https://doi.org/10.1002/smll.202106401	journal	January 2022
Understanding protein adsorption phenomena at solid surfaces Rabe, Michael; Verdes, Dorinel; Seeger, Stefan Advances in Colloid and Interface Science, Vol. 162, Issue 1-2 https://doi.org/10.1016/j.cis.2010.12.007	journal	February 2011
A bottom-up approach to understanding protein layer formation at solid–liquid interfaces Kastantin, Mark; Langdon, Blake B.; Schwartz, Daniel K. Advances in Colloid and Interface Science, Vol. 207 https://doi.org/10.1016/j.cis.2013.12.006	journal	May 2014
Multiparametric AFM insights into electron transport mechanisms in biomemristors Shi, Chenyang; Heble, Annie Y.; Zhang, Shuai Materials Today Physics, Vol. 44 https://doi.org/10.1016/j.mtphys.2024.101429	journal	May 2024
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
A review of biomimetic surface functionalization for bone-integrating orthopedic implants: Mechanisms, current approaches, and future directions Stewart, Callum; Akhavan, Behnam; Wise, Steven G. Progress in Materials Science, Vol. 106 https://doi.org/10.1016/j.pmatsci.2019.100588	journal	December 2019
Biocompatible polymer materials: Role of protein–surface interactions Chen, Hong; Yuan, Lin; Song, Wei Progress in Polymer Science, Vol. 33, Issue 11 https://doi.org/10.1016/j.progpolymsci.2008.07.006	journal	November 2008
Redox Interfaces for Electrochemically Controlled Protein–Surface Interactions: Bioseparations and Heterogeneous Enzyme Catalysis Su, Xiao; Hübner, Jonas; Kauke, Monique J. Chemistry of Materials, Vol. 29, Issue 13 https://doi.org/10.1021/acs.chemmater.7b01699	journal	June 2017
Moving beyond the Solvent-Tip Approximation to Determine Site-Specific Variations of Interfacial Water Structure through 3D Force Microscopy Nakouzi, Elias; Stack, Andrew G.; Kerisit, Sebastien The Journal of Physical Chemistry C, Vol. 125, Issue 2 https://doi.org/10.1021/acs.jpcc.0c07901	journal	December 2020
Water Adsorption on Mica Surfaces with Hydrophilicity Tuned by Counterion Types (Na, K, and Cs) and Structural Fluorination Koishi, Ayumi; Lee, Sang Soo; Fenter, Paul The Journal of Physical Chemistry C, Vol. 126, Issue 38 https://doi.org/10.1021/acs.jpcc.2c04751	journal	September 2022
Solution Structure and Hydration Forces between Mica and Hydrophilic Versus Hydrophobic Surfaces Nakouzi, E.; Kerisit, S.; Legg, B. A. The Journal of Physical Chemistry C, Vol. 127, Issue 5, p. 2741-2752 https://doi.org/10.1021/acs.jpcc.2c09120	journal	January 2023
Effect of Ions on Solution Structure and Hydration Forces at the Orthoclase–Water Interface Nakouzi, Elias; Kerisit, Sebastien N.; Heo, Jaeyoung The Journal of Physical Chemistry C, Vol. 129, Issue 15 https://doi.org/10.1021/acs.jpcc.5c01034	journal	April 2025
Discrete Orientations of Interfacial Waters Direct Crystallization of Mica-Binding Proteins Alberstein, Robert G.; Prelesnik, Jesse L.; Nakouzi, Elias The Journal of Physical Chemistry Letters, Vol. 14, Issue 1 https://doi.org/10.1021/acs.jpclett.2c02948	journal	December 2022
Role of Mono- and Divalent Surface Cations on the Structure and Adsorption Behavior of Water on Mica Surface Adapa, Sai; Swamy, Dhananjay R.; Kancharla, Samhitha Langmuir, Vol. 34, Issue 48 https://doi.org/10.1021/acs.langmuir.8b01128	journal	November 2018
Ion-Specific and pH-Dependent Hydration of Mica–Electrolyte Interfaces van Lin, Simone R.; Grotz, Kara K.; Siretanu, Igor Langmuir, Vol. 35, Issue 17 https://doi.org/10.1021/acs.langmuir.9b00520	journal	April 2019
Effect of Functional Groups of Self-Assembled Monolayers on Protein Adsorption and Initial Cell Adhesion Hasan, Abshar; Pattanayek, Sudip K.; Pandey, Lalit M. ACS Biomaterials Science & Engineering, Vol. 4, Issue 9 https://doi.org/10.1021/acsbiomaterials.8b00795	journal	August 2018
Disentangling Rotational Dynamics and Ordering Transitions in a System of Self-Organizing Protein Nanorods via Rotationally Invariant Latent Representations Kalinin, Sergei V.; Zhang, Shuai; Valleti, Mani ACS Nano, Vol. 15, Issue 4 https://doi.org/10.1021/acsnano.0c08914	journal	April 2021
In Operando Imaging Electrostatic-Driven Disassembly and Reassembly of Collagen Nanostructures Garcia-Sacristan, Clara; Gisbert, Victor G.; Klein, Kevin ACS Nano, Vol. 18, Issue 28 https://doi.org/10.1021/acsnano.4c03839	journal	July 2024
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
Biomolecular Structure at Solid–Liquid Interfaces As Revealed by Nonlinear Optical Spectroscopy Roy, Sandra; Covert, Paul A.; FitzGerald, William R. Chemical Reviews, Vol. 114, Issue 17 https://doi.org/10.1021/cr400418b	journal	January 2014
Template-Directed Assembly of a de Novo Designed Protein Brown, Christina L.; Aksay, Ilhan A.; Saville, Dudley A. Journal of the American Chemical Society, Vol. 124, Issue 24 https://doi.org/10.1021/ja0261271	journal	June 2002
Direct Observation of the Orientational Anisotropy of Buried Hydroxyl Groups inside Muscovite Mica Tuladhar, Aashish; Chase, Zizwe A.; Baer, Marcel D. Journal of the American Chemical Society, Vol. 141, Issue 5 https://doi.org/10.1021/jacs.8b12483	journal	January 2019
A Survey of Structure−Property Relationships of Surfaces that Resist the Adsorption of Protein Ostuni, Emanuele; Chapman, Robert G.; Holmlin, R. Erik Langmuir, Vol. 17, Issue 18 https://doi.org/10.1021/la010384m	journal	September 2001
Highly Selective Protein Patterning on Gold−Silicon Substrates for Biosensor Applications Veiseh, Mandana; Zareie, M. Hadi; Zhang, Miqin Langmuir, Vol. 18, Issue 17 https://doi.org/10.1021/la025529j	journal	July 2002
Self-Assembly of Collagen on Flat Surfaces: The Interplay of Collagen–Collagen and Collagen–Substrate Interactions Narayanan, Badri; Gilmer, George H.; Tao, Jinhui Langmuir, Vol. 30, Issue 5 https://doi.org/10.1021/la4043364	journal	January 2014
Mica Surface Promotes the Assembly of Cytoskeletal Proteins Hamon, Loic; Panda, Dulal; Savarin, Philippe Langmuir, Vol. 25, Issue 6 https://doi.org/10.1021/la8035743	journal	February 2009
Structural and Thermodynamic Explanations of Ostwald's Rule Threlfall, Terry Organic Process Research & Development, Vol. 7, Issue 6 https://doi.org/10.1021/op030026l	journal	November 2003
Degradable polyester scaffolds with controlled surface chemistry combining minimal protein adsorption with specific bioactivation Grafahrend, Dirk; Heffels, Karl-Heinz; Beer, Meike V. Nature Materials, Vol. 10, Issue 1 https://doi.org/10.1038/nmat2904	journal	December 2010
Tuning crystallization pathways through sequence engineering of biomimetic polymers Ma, Xiang; Zhang, Shuai; Jiao, Fang Nature Materials, Vol. 16, Issue 7 https://doi.org/10.1038/nmat4891	journal	April 2017
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
Macroscale-area patterning of three-dimensional DNA-programmable frameworks Teng, Feiyue; Zhang, Honghu; Nykypanchuk, Dmytro Nature Communications, Vol. 16, Issue 1 https://doi.org/10.1038/s41467-025-58422-0	journal	April 2025
Regulation of membrane protein structure and function by their lipid nano-environment Levental, Ilya; Lyman, Ed Nature Reviews Molecular Cell Biology, Vol. 24, Issue 2 https://doi.org/10.1038/s41580-022-00524-4	journal	September 2022
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
The two-step mechanism of nucleation of crystals in solution Vekilov, Peter G. Nanoscale, Vol. 2, Issue 11 https://doi.org/10.1039/c0nr00628a	journal	January 2010
Hierarchical ordering of amyloid fibrils on the mica surface Zhou, Xingfei; Zhang, Yingying; Zhang, Feng Nanoscale, Vol. 5, Issue 11 https://doi.org/10.1039/c3nr00886j	journal	January 2013
Thermodynamically consistent description of the work to form a nucleus of any size Kashchiev, Dimo The Journal of Chemical Physics, Vol. 118, Issue 4 https://doi.org/10.1063/1.1531614	journal	January 2003
Interfacial water on collagen nanoribbons by 3D AFM Arvelo, Diana M.; Garcia-Sacristan, Clara; Chacón, Enrique The Journal of Chemical Physics, Vol. 160, Issue 16 https://doi.org/10.1063/5.0205611	journal	April 2024
Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics Chung, S.; Shin, S. -H.; Bertozzi, C. R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 38 https://doi.org/10.1073/pnas.1008280107	journal	September 2010
Rotational dynamics and transition mechanisms of surface-adsorbed proteins Zhang, Shuai; Sadre, Robbie; Legg, Benjamin A. Proceedings of the National Academy of Sciences, Vol. 119, Issue 16 https://doi.org/10.1073/pnas.2020242119	journal	April 2022
Ion-dependent protein–surface interactions from intrinsic solvent response Prelesnik, Jesse L.; Alberstein, Robert G.; Zhang, Shuai Proceedings of the National Academy of Sciences, Vol. 118, Issue 26 https://doi.org/10.1073/pnas.2025121118	journal	June 2021
A review of protein adsorption on bioceramics Wang, Kefeng; Zhou, Changchun; Hong, Youliang Interface Focus, Vol. 2, Issue 3 https://doi.org/10.1098/rsfs.2012.0012	journal	March 2012
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
Two-dimensional silk Shi, Chenyang; Zorman, Marlo; Zhao, Xiao Science Advances, Vol. 10, Issue 38 https://doi.org/10.1126/sciadv.ado4142	journal	September 2024
De novo design of self-assembling helical protein filaments Shen, Hao; Fallas, Jorge A.; Lynch, Eric Science, Vol. 362, Issue 6415 https://doi.org/10.1126/science.aau3775	journal	November 2018
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
Studien über die Bildung und Umwandlung fester Körper Ostwald, W. Zeitschrift für Physikalische Chemie, Vol. 22U, Issue 1 https://doi.org/10.1515/zpch-1897-2233	journal	January 1897
Mica Lattice Orientation of Epitaxially Grown Amyloid β25–35 Fibrils Ferenczy, György G.; Murvai, Ünige; Fülöp, Lívia International Journal of Molecular Sciences, Vol. 25, Issue 19 https://doi.org/10.3390/ijms251910460	journal	September 2024

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