Thermodynamic Analysis of Silk Fibroin–Graphite Hybrid Materials and Their Morphology

Zorman, Marlo; Phillips, Christian; Shi, Chenyang; Zhang, Shuai; De Yoreo, James; Pfaendtner, Jim

doi:10.1021/acs.jpcb.3c08147

Thermodynamic Analysis of Silk Fibroin–Graphite Hybrid Materials and Their Morphology

Journal Article · Wed Feb 28 23:00:00 EST 2024 · Journal of Physical Chemistry. B

DOI:https://doi.org/10.1021/acs.jpcb.3c08147· OSTI ID:2406995

^[1]; Phillips, Christian ^[1]; Shi, Chenyang ^[2]; ^[2]; ^[2]; ^[3]

Univ. of Washington, Seattle, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Univ. of Washington, Seattle, WA (United States)
Univ. of Washington, Seattle, WA (United States); North Carolina State University, Raleigh, NC (United States)

Silk fibroin (SF) is a β-sheet-rich protein that is responsible for the remarkable tensile strength of silk. In addition to its mechanical properties, SF is biocompatible and biodegradable, making it an attractive candidate for use in biotic/abiotic hybrid materials. A pairing of particular interest is the use of SF with graphene-based nanomaterials (GBNs). The properties of this interface drive the formation of well-ordered nanostructures and can improve the electronic properties of the resulting hybrid. It was previously demonstrated that SF can form lamellar nanostructures in the presence of graphite; however, the equilibrium morphology and associated driving interactions are not fully understood. Here, in this study, we characterize these interactions between SF and SF lamellar with graphite using molecular dynamics (MD) simulations and umbrella sampling (US). We find that SF lamellar nanostructures have strong orientational and spatial preferences on graphite that are driven by the hydrophobic effect, destabilizing solvent–protein interactions and stabilizing protein–protein and protein–graphite interactions. Finally, we show how careful consideration of these underlying interactions can be applied to rationally modify the nanostructure morphology.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division (MSE)

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

OSTI ID:: 2406995

Report Number(s):: PNNL-SA--193525

Journal Information:: Journal of Physical Chemistry. B, Journal Name: Journal of Physical Chemistry. B Journal Issue: 10 Vol. 128; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (48)

LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H	journal	September 1997
Silk Fibroin-Substrate Interactions at Heterogeneous Nanocomposite Interfaces Grant, Anise M.; Kim, Ho Shin; Dupnock, Trisha L. Advanced Functional Materials, Vol. 26, Issue 35 https://doi.org/10.1002/adfm.201601268	journal	July 2016
Design, Fabrication, and Function of Silk-Based Nanomaterials Wang, Yu; Guo, Jin; Zhou, Liang Advanced Functional Materials, Vol. 28, Issue 52 https://doi.org/10.1002/adfm.201805305	journal	November 2018
Ultra-Robust Graphene Oxide-Silk Fibroin Nanocomposite Membranes Hu, Kesong; Gupta, Maneesh K.; Kulkarni, Dhaval D. Advanced Materials, Vol. 25, Issue 16 https://doi.org/10.1002/adma.201300179	journal	March 2013
Engineering Multi‐Scale Organization for Biotic and Organic Abiotic Electroactive Systems Yao, Ze‐Fan; Lundqvist, Emil; Kuang, Yuyao Advanced Science, Vol. 10, Issue 10 https://doi.org/10.1002/advs.202205381	journal	January 2023
Metal‐Free Semiconductor‐Based Bio‐Nano Hybrids for Sustainable CO ₂ ‐to‐CH ₄ Conversion with High Quantum Yield Hu, Andong; Ye, Jie; Ren, Guoping Angewandte Chemie, Vol. 134, Issue 35 https://doi.org/10.1002/ange.202206508	journal	July 2022
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
PACKMOL: A package for building initial configurations for molecular dynamics simulations Martínez, L.; Andrade, R.; Birgin, E. G. Journal of Computational Chemistry, Vol. 30, Issue 13 https://doi.org/10.1002/jcc.21224	journal	October 2009
Biomaterials for Tissue Engineering Lee, Esther J.; Kasper, F. Kurtis; Mikos, Antonios G. Annals of Biomedical Engineering, Vol. 42, Issue 2 https://doi.org/10.1007/s10439-013-0859-6	journal	July 2013
Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling Torrie, G. M.; Valleau, J. P. Journal of Computational Physics, Vol. 23, Issue 2 https://doi.org/10.1016/0021-9991(77)90121-8	journal	February 1977
Structure–function–property–design interplay in biopolymers: Spider silk Tokareva, Olena; Jacobsen, Matthew; Buehler, Markus Acta Biomaterialia, Vol. 10, Issue 4 https://doi.org/10.1016/j.actbio.2013.08.020	journal	April 2014
MDTraj: A Modern Open Library for the Analysis of Molecular Dynamics Trajectories McGibbon, Robert T.; Beauchamp, Kyle A.; Harrigan, Matthew P. Biophysical Journal, Vol. 109, Issue 8 https://doi.org/10.1016/j.bpj.2015.08.015	journal	October 2015
Surfactant self-assembly structures and multilayer formation at the solid-solution interface induces by electrolyte, polymers and proteins Petkov, Jordan T.; Penfold, Jeffery; Thomas, Robert K. Current Opinion in Colloid & Interface Science, Vol. 57 https://doi.org/10.1016/j.cocis.2021.101541	journal	February 2022
PLUMED 2: New feathers for an old bird Tribello, Gareth A.; Bonomi, Massimiliano; Branduardi, Davide Computer Physics Communications, Vol. 185, Issue 2 https://doi.org/10.1016/j.cpc.2013.09.018	journal	February 2014
Functionalization of graphene-based nanomaterials for energy and hydrogen storage Boateng, Emmanuel; Thiruppathi, Antony R.; Hung, Chi-Kai Electrochimica Acta, Vol. 452 https://doi.org/10.1016/j.electacta.2023.142340	journal	June 2023
Tunable green graphene-silk biomaterials: Mechanism of protein-based nanocomposites Wang, Fang; Jyothirmayee Aravind, S. S.; Wu, Hao Materials Science and Engineering: C, Vol. 79 https://doi.org/10.1016/j.msec.2017.05.120	journal	October 2017
Structures, mechanical properties and applications of silk fibroin materials Koh, Leng-Duei; Cheng, Yuan; Teng, Choon-Peng Progress in Polymer Science, Vol. 46 https://doi.org/10.1016/j.progpolymsci.2015.02.001	journal	July 2015
Recent progress of graphene based nanomaterials in bioelectrochemical systems Olabi, A. G.; Wilberforce, Tabbi; Sayed, Enas Taha Science of The Total Environment, Vol. 749 https://doi.org/10.1016/j.scitotenv.2020.141225	journal	December 2020
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
Synergistic Integration of Experimental and Simulation Approaches for the de Novo Design of Silk-Based Materials Huang, Wenwen; Ebrahimi, Davoud; Dinjaski, Nina Accounts of Chemical Research, Vol. 50, Issue 4 https://doi.org/10.1021/acs.accounts.6b00616	journal	February 2017
How Does Nature Evade the “Larger is Weaker” Fate of Ultralong Silk β-Sheet Nanocrystallites Li, Dechang; Wang, Qianchun; Xu, Changjian Nano Letters, Vol. 20, Issue 12 https://doi.org/10.1021/acs.nanolett.0c02968	journal	October 2020
Peptide–Graphene Interactions Enhance the Mechanical Properties of Silk Fibroin Cheng, Yuan; Koh, Leng-Duei; Li, Dechang ACS Applied Materials & Interfaces, Vol. 7, Issue 39 https://doi.org/10.1021/acsami.5b05615	journal	September 2015
Silk Fibroin as a Green Material DeBari, Megan K.; King, Claude I.; Altgold, Tahlia A. ACS Biomaterials Science & Engineering, Vol. 7, Issue 8 https://doi.org/10.1021/acsbiomaterials.1c00493	journal	July 2021
Adsorption Behavior of Silk Fibroin on Amphiphilic Graphene Oxide Tadepalli, Sirimuvva; Hamper, Henry; Park, Sang Hyun ACS Biomaterials Science & Engineering, Vol. 2, Issue 7 https://doi.org/10.1021/acsbiomaterials.6b00232	journal	June 2016
Silk-Templated Nanomaterial Interfaces for Wearables and Bioelectronics: Advances and Prospects Ahmed, Abbas; Bain, Sudipta; Prottoy, Zawad Hasan ACS Materials Letters, Vol. 4, Issue 1 https://doi.org/10.1021/acsmaterialslett.1c00618	journal	December 2021
Template-Guided Assembly of Silk Fibroin on Cellulose Nanofibers for Robust Nanostructures with Ultrafast Water Transport Xiong, Rui; Kim, Ho Shin; Zhang, Shuaidi ACS Nano, Vol. 11, Issue 12 https://doi.org/10.1021/acsnano.7b04235	journal	October 2016
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
Crystalline Regions of Bombyx mori Silk Fibroin May Exhibit β-Turn and β-Helix Conformations Lazo, N. D.; Downing, Donald T. Macromolecules, Vol. 32, Issue 14 https://doi.org/10.1021/ma9900582	journal	June 1999
Structure of Graphite Freise, E. J. Nature, Vol. 193, Issue 4816 https://doi.org/10.1038/193671a0	journal	February 1962
Uncovering the structure–function relationship in spider silk Yarger, Jeffery L.; Cherry, Brian R.; van der Vaart, Arjan Nature Reviews Materials, Vol. 3, Issue 3 https://doi.org/10.1038/natrevmats.2018.8	journal	March 2018
CHARMM36m: an improved force field for folded and intrinsically disordered proteins Huang, Jing; Rauscher, Sarah; Nawrocki, Grzegorz Nature Methods, Vol. 14, Issue 1 https://doi.org/10.1038/nmeth.4067	journal	November 2016
Materials fabrication from Bombyx mori silk fibroin Rockwood, Danielle N.; Preda, Rucsanda C.; Yücel, Tuna Nature Protocols, Vol. 6, Issue 10 https://doi.org/10.1038/nprot.2011.379	journal	September 2011
Array programming with NumPy Harris, Charles R.; Millman, K. Jarrod; van der Walt, Stéfan J. Nature, Vol. 585, Issue 7825 https://doi.org/10.1038/s41586-020-2649-2	journal	September 2020
A modified TIP3P water potential for simulation with Ewald summation Price, Daniel J.; Brooks, Charles L. The Journal of Chemical Physics, Vol. 121, Issue 20 https://doi.org/10.1063/1.1808117	journal	November 2004
Statistically optimal analysis of samples from multiple equilibrium states Shirts, Michael R.; Chodera, John D. The Journal of Chemical Physics, Vol. 129, Issue 12 https://doi.org/10.1063/1.2978177	journal	September 2008
Molecular dynamics with coupling to an external bath Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F. The Journal of Chemical Physics, Vol. 81, Issue 8 https://doi.org/10.1063/1.448118	journal	October 1984
The Nose–Hoover thermostat Evans, D. J.; Holian, B. L. The Journal of Chemical Physics, Vol. 83, Issue 8 https://doi.org/10.1063/1.449071	journal	October 1985
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Generalized Verlet Algorithm for Efficient Molecular Dynamics Simulations with Long-range Interactions Grubmüller, H.; Heller, H.; Windemuth, A. Molecular Simulation, Vol. 6, Issue 1-3 https://doi.org/10.1080/08927029108022142	journal	March 1991
On the strength of β-sheet crystallites of Bombyx mori silk fibroin Cheng, Yuan; Koh, Leng-Duei; Li, Dechang Journal of The Royal Society Interface, Vol. 11, Issue 96 https://doi.org/10.1098/rsif.2014.0305	journal	July 2014
Matplotlib: A 2D Graphics Environment Hunter, John D. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.55	journal	January 2007
Biomaterials: Been There, Done That, and Evolving into the Future Ratner, Buddy D. Annual Review of Biomedical Engineering, Vol. 21, Issue 1 https://doi.org/10.1146/annurev-bioeng-062117-120940	journal	June 2019
Challenges in Development of Nanoparticle-Based Therapeutics Desai, Neil The AAPS Journal, Vol. 14, Issue 2 https://doi.org/10.1208/s12248-012-9339-4	journal	March 2012
MDAnalysis: A Python Package for the Rapid Analysis of Molecular Dynamics Simulations Gowers, Richard; Linke, Max; Barnoud, Jonathan Proceedings of the Python in Science Conference https://doi.org/10.25080/Majora-629e541a-00e	conference	January 2016
Challenges With the Development of Biomaterials for Sustainable Tissue Engineering Williams, David F. Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00127	journal	May 2019
An Overview of Functionalized Graphene Nanomaterials for Advanced Applications Maio, Andrea; Pibiri, Ivana; Morreale, Marco Nanomaterials, Vol. 11, Issue 7 https://doi.org/10.3390/nano11071717	journal	June 2021
Fabrication of Silk Fibroin/Graphene Film with High Electrical Conductivity and Humidity Sensitivity Zhang, Haoran; Zhao, Juntao; Xing, Tieling Polymers, Vol. 11, Issue 11 https://doi.org/10.3390/polym11111774	journal	October 2019
Silk Fibroin-Based Biomaterials for Biomedical Applications: A Review Nguyen, Thang Phan; Nguyen, Quang Vinh; Nguyen, Van-Huy Polymers, Vol. 11, Issue 12 https://doi.org/10.3390/polym11121933	journal	November 2019

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