Skip to main content
SpringerLink
Log in

Interfacial interactions between spider silk protein and cellulose studied by molecular dynamics simulation

  • Original Paper
  • Published:
Journal of Molecular Modeling Aims and scope Submit manuscript

Abstract

Context

Due to their excellent biocompatibility and degradability, cellulose/spider silk protein composites hold a significant value in biomedical applications such as tissue engineering, drug delivery, and medical dressings. The interfacial interactions between cellulose and spider silk protein affect the properties of the composite. Therefore, it is important to understand the interfacial interactions between spider silk protein and cellulose to guide the design and optimization of composites. The study of the adsorption of protein on specific surfaces of cellulose crystal can be very complex using experimental methods. Molecular dynamics simulations allow the exploration of various physical and chemical changes at the atomic level of the material and enable an atomic description of the interactions between cellulose crystal planes and spider silk protein. In this study, molecular dynamics simulations were employed to investigate the interfacial interactions between spider silk protein (NTD) and cellulose surfaces. Findings of RMSD, RMSF, and secondary structure showed that the structure of NTD proteins remained unchanged during the adsorption process. Cellulose contact numbers and hydrogen bonding trends on different crystalline surfaces suggest that van der Waals forces and hydrogen bonding interactions drive the binding of proteins to cellulose. These findings reveal the interaction between cellulose and protein at the molecular level and provide theoretical guidance for the design and synthesis of cellulose/spider silk protein composites.

Methods

MD simulations were all performed using the GROMACS-5.1 software package and run with CHARMM36 carbohydrate force field. Molecular dynamics simulations were performed for 500 ns for the simulated system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Data availability

Data will be made available on request.

References

  1. Bhat A, Khan I, Usmani MA, Umapathi R, Al-Kindy SM (2019) Cellulose an ageless renewable green nanomaterial for medical applications: an overview of ionic liquids in extraction, separation and dissolution of cellulose. Int J Biol Macromol 129:750–777. https://doi.org/10.1016/j.ijbiomac.2018.12.190

    Article  CAS  PubMed  Google Scholar 

  2. Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23(9):545–557. https://doi.org/10.1016/j.tim.2015.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Abdelhamid HN, Mathew AP (2021) Cellulose-based materials for water remediation: adsorption, catalysis, and antifouling. Front Chem Eng 3:790314. https://doi.org/10.3389/fceng.2021.790314

    Article  Google Scholar 

  4. Akturk A (2023) Enrichment of cellulose acetate nanofibrous scaffolds with retinyl palmitate and clove essential oil for wound healing applications. ACS Omega 8(6):5553–5560. https://doi.org/10.1021/acsomega.2c06881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mohamed MA, Abd Mutalib M, Hir ZAM, Zain M, Mohamad AB, Minggu LJ, Awang NA, Salleh W (2017) An overview on cellulose-based material in tailoring bio-hybrid nanostructured photocatalysts for water treatment and renewable energy applications. Int J Biol Macromol 103:1232–1256. https://doi.org/10.1016/j.ijbiomac.2017.05.181

    Article  CAS  PubMed  Google Scholar 

  6. Ghalei S, Douglass M, Handa H (2022) Nitric oxide-releasing nanofibrous scaffolds based on silk fibroin and zein with enhanced biodegradability and antibacterial properties. ACS Biomater Sci Eng 8(7):3066–3077. https://doi.org/10.1021/acsbiomaterials.2c00103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Rising A, Johansson J (2015) Toward spinning artificial spider silk. Nat Chem Biol 11(5):309–315. https://doi.org/10.1038/nchembio.1789

    Article  CAS  PubMed  Google Scholar 

  8. Vollrath F, Knight D (1999) Structure and function of the silk production pathway in the spider Nephila edulis. Int J Biol Macromol 24(2–3):243–249. https://doi.org/10.1016/S0141-8130(98)00095-6

    Article  CAS  PubMed  Google Scholar 

  9. Wendt H, Hillmer A, Reimers K, Kuhbier JW, Schäfer-Nolte F, Allmeling C, Kasper C, Vogt PM (2011) Artificial skin–culturing of different skin cell lines for generating an artificial skin substitute on cross-weaved spider silk fibres. PLoS ONE 6(7):e21833. https://doi.org/10.1371/journal.pone.0021833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Allmeling C, Jokuszies A, Reimers K, Kall S, Choi C, Brandes G, Kasper C, Scheper T, Guggenheim M, Vogt P (2008) Spider silk fibres in artificial nerve constructs promote peripheral nerve regeneration. Cell Prolif 41(3):408–420. https://doi.org/10.1111/j.1365-2184.2008.00534.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gellynck K, Verdonk PC, Van Nimmen E, Almqvist KF, Gheysens T, Schoukens G, Van Langenhove L, Kiekens P, Mertens J, Verbruggen G (2008) Silkworm and spider silk scaffolds for chondrocyte support. J Mater Sci Mater Med 19:3399–3409. https://doi.org/10.1007/s10856-008-3474-6

    Article  CAS  PubMed  Google Scholar 

  12. SM Choi, P Chaudhry, SM Zo and SS Han (2018) Advances in protein-based materials: from origin to novel biomaterials. Cutting-edge enabling technologies for regenerative medicine:161–210.https://doi.org/10.1007/978-981-13-0950-2_10

  13. Lawrence BD, Marchant JK, Pindrus MA, Omenetto FG, Kaplan DL (2009) Silk film biomaterials for cornea tissue engineering. Biomaterials 30(7):1299–1308. https://doi.org/10.1002/macp.202170013

    Article  CAS  PubMed  Google Scholar 

  14. Kundu B, Rajkhowa R, Kundu SC, Wang X (2013) Silk fibroin biomaterials for tissue regenerations. Adv. Drug Delivery Rev. 65(4):457–470. https://doi.org/10.1016/j.addr.2012.09.043

    Article  CAS  Google Scholar 

  15. Harris TI, Gaztambide DA, Day BA, Brock CL, Ruben AL, Jones JA, Lewis RV (2016) Sticky situation: an investigation of robust aqueous-based recombinant spider silk protein coatings and adhesives. Biomacromolecules 17(11):3761–3772. https://doi.org/10.1021/acs.biomac.6b01267

    Article  CAS  PubMed  Google Scholar 

  16. Lewicka M, Hermanson O, Rising AU (2012) Recombinant spider silk matrices for neural stem cell cultures. Biomaterials 33(31):7712–7717. https://doi.org/10.1016/j.biomaterials.2012.07.021

    Article  CAS  PubMed  Google Scholar 

  17. Franco AR, Fernandes EM, Rodrigues MT, Rodrigues FJ, Gomes ME, Leonor IB, Kaplan DL, Reis RL (2019) Antimicrobial coating of spider silk to prevent bacterial attachment on silk surgical sutures. Acta Biomater. 99:236–246. https://doi.org/10.1016/j.actbio.2019.09.004

    Article  CAS  PubMed  Google Scholar 

  18. Allardyce BJ, Rajkhowa R, Dilley RJ, Redmond SL, Atlas MD, Wang X (2017) Glycerol-plasticised silk membranes made using formic acid are ductile, transparent and degradation-resistant. Mater. Sci. Eng C 80:165–173. https://doi.org/10.1016/j.msec.2017.05.112

    Article  CAS  Google Scholar 

  19. Mohammadi P, Beaune GG, Stokke BT, Timonen JV, Linder MB (2018) Self-coacervation of a silk-like protein and its use as an adhesive for cellulosic materials. ACS macro letters 7(9):1120–1125. https://doi.org/10.1021/acsmacrolett.8b00527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mohammadi P, Aranko AS, Landowski CP, Ikkala O, Jaudzems K, Wagermaier W, Linder MB (2019) Biomimetic composites with enhanced toughening using silk-inspired triblock proteins and aligned nanocellulose reinforcements. Sci Adv 5(9):2541. https://doi.org/10.1126/sciadv.aaw2541

    Article  CAS  Google Scholar 

  21. Meirovitch S, Shtein Z, Ben-Shalom T, Lapidot S, Tamburu C, Hu X, Kluge JA, Raviv U, Kaplan DL, Shoseyov O (2016) Spider silk-CBD-cellulose nanocrystal composites: mechanism of assembly. Int J Mol Sci 17(9):1573. https://doi.org/10.3390/ijms17091573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lemetti L, Tersteegen J, Sammaljarvi J, Aranko AS, Linder MB, Engineering (2021) Recombinant spider silk protein and delignified wood form a strong adhesive system. ACS Sustain Chem Eng 10(1):552–561. https://doi.org/10.1021/acssuschemeng.1c07043

    Article  CAS  Google Scholar 

  23. Voutilainen S, Paananen A, Lille M, Linder MB (2019) Modular protein architectures for pH-dependent interactions and switchable assembly of nanocellulose. Int J Biol Macromol 137:270–276. https://doi.org/10.1016/j.ijbiomac.2019.06.227

    Article  CAS  PubMed  Google Scholar 

  24. Jesson DA, Watts JF (2012) The interface and interphase in polymer matrix composites: effect on mechanical properties and methods for identification. Polym Rev (Philadelphia, PA, U.S) 52(3):321–354. https://doi.org/10.1080/15583724.2012.710288

    Article  CAS  Google Scholar 

  25. Muthoka RM, Panicker PS, Kim J (2022) Molecular dynamics study of cellulose nanofiber alignment under an electric field. Polymers 14(9):1925. https://doi.org/10.3390/polym14091925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Atkison JH, Parnham S, Marcotte WR, Olsen SK (2016) Crystal structure of the nephila clavipes major ampullate spidroin 1A N-terminal domain reveals plasticity at the dimer interface. J. Biol. Chem. 291(36):19006–19017. https://doi.org/10.1074/jbc.M116.736710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Vermaas JV, Crowley MF, Beckham GT, Engineering (2019) A quantitative molecular atlas for interactions between lignin and cellulose. ACS Sustain Chem Eng 7(24):19570–19583. https://doi.org/10.1021/acssuschemeng.9b04648

    Article  CAS  Google Scholar 

  28. Malaspina DC, Faraudo J (2019) Molecular insight into the wetting behavior and amphiphilic character of cellulose nanocrystals. Adv Colloid Interface Sci 267:15–25. https://doi.org/10.1016/j.cis.2019.02.003

    Article  CAS  PubMed  Google Scholar 

  29. Ren Z, Guo R, Bi H, Jia X, Xu M, Cai L, Interfaces (2019) Interfacial adhesion of polylactic acid on cellulose surface: a molecular dynamics study. ACS Appl Mater Interfaces 12(2):3236–3244. https://doi.org/10.1021/acsami.9b20101

    Article  CAS  Google Scholar 

  30. Gomes TC, Skaf MS (2012) Cellulose-builder: a toolkit for building crystalline structures of cellulose. J Comput Chem 33(14):1338–1346. https://doi.org/10.1002/jcc.22959

    Article  CAS  PubMed  Google Scholar 

  31. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125(47):14300–14306. https://doi.org/10.1021/ja037055w

    Article  CAS  PubMed  Google Scholar 

  32. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124(31):9074–9082. https://doi.org/10.1021/ja0257319

    Article  CAS  PubMed  Google Scholar 

  33. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(1):33–38. https://doi.org/10.1016/0263-7855(96)00018-5

    Article  CAS  PubMed  Google Scholar 

  34. Boonstra S, Onck PR, van der Giessen E (2016) CHARMM TIP3P water model suppresses peptide folding by solvating the unfolded state. J Phys Chem B 120(15):3692–3698. https://doi.org/10.1021/acs.jpcb.6b01316

    Article  CAS  PubMed  Google Scholar 

  35. Liu Y, Song X, Yang Y (2020) Anisotropic protein diffusion on nanosurface. Nanoscale 12(8):5209–5216. https://doi.org/10.1039/c9nr08555f

    Article  CAS  PubMed  Google Scholar 

  36. Ge C, Du J, Zhao L, Wang L, Liu Y, Li D (2011) Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc Natl Acad Sci U.S.A 108(41):16968–16973. https://doi.org/10.1073/pnas.1105270108

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ma H, Shi Q, Li X, Ren J, Wang Y, Li Z, Ning L (2023) Molecular and thermodynamic insights into interfacial interactions between collagen and cellulose investigated by molecular dynamics simulation and umbrella sampling. J Comput-Aided Mol Des 37(1):39–51. https://doi.org/10.1007/s10822-022-00489-8

    Article  CAS  PubMed  Google Scholar 

  38. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ (2005) GROMACS: fast, flexible, and free. J Comput Chem 26(16):1701–1718. https://doi.org/10.1002/jcc.20291

    Article  CAS  PubMed  Google Scholar 

  39. Berendsen HJ, van der Spoel D, van Drunen R (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Comput Phys Commun 91(1–3):43–56. https://doi.org/10.1016/0010-4655(95)00042-E

    Article  CAS  Google Scholar 

  40. Lee S, Tran A, Allsopp M, Lim JB, Hénin J, Klauda JB (2014) CHARMM36 united atom chain model for lipids and surfactants. J Phys Chem B 118(2):547–556. https://doi.org/10.1021/jp410344g

    Article  CAS  PubMed  Google Scholar 

  41. French AD (2017) Glucose, not cellobiose, is the repeating unit of cellulose and why that is important. Cellulose 24:4605–4609. https://doi.org/10.1007/s10570-017-1450-3

    Article  CAS  Google Scholar 

  42. Petersen HG (1995) Accuracy and efficiency of the particle mesh Ewald method. J Chem Phys 103(9):3668–3679. https://doi.org/10.1063/1.470043

    Article  CAS  Google Scholar 

  43. Hess B, Bekker H, Berendsen HJ, Fraaije JG (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18(12):1463–1472

    Article  CAS  Google Scholar 

  44. Berendsen HJ, Postma JV, Van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81(8):3684–3690. https://doi.org/10.1063/1.448118

    Article  CAS  Google Scholar 

  45. Parrinello M, Rahman A (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52(12):7182–7190. https://doi.org/10.1063/1.328693

    Article  CAS  Google Scholar 

  46. Parrinello M, Rahman A (1998) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52(12):7182–7190. https://doi.org/10.1063/1.328693

    Article  Google Scholar 

  47. Hub JS (2015) g_wham—a free weighted histogram analysis implementation including robust error and autocorrelation estimates. J Chem Phys 6(9):3713–3720. https://doi.org/10.1063/1.4931819

    Article  CAS  Google Scholar 

  48. Hooft RW, Sander C, Vriend G (1997) Objectively judging the quality of a protein structure from a Ramachandran plot. Comput Appl Biosci 13(4):425–430. https://doi.org/10.1093/bioinformatics/13.4.425

    Article  CAS  PubMed  Google Scholar 

  49. Sargsyan K, Grauffel C, Lim C (2017) How molecular size impacts RMSD applications in molecular dynamics simulations. J Chem Theory Comput. 13(4):1518–1524. https://doi.org/10.1021/acs.jctc.7b00028

    Article  CAS  PubMed  Google Scholar 

  50. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolym Orig Res Biomol 22(12):2577–2637. https://doi.org/10.1002/bip.360221211

    Article  CAS  Google Scholar 

  51. Feng Q, Noumbissi R, Biswas K, Koizumi H (2017) The role of hydroxyl groups in interchain interactions in cellulose Iα and Iβ. Int J Quantum Chem 117(10):e25357. https://doi.org/10.1002/qua.25357

    Article  CAS  Google Scholar 

  52. Xu Y, Gao M, Zhang Y, Ning L, Zhao D, Ni Y (2022) Cellulose hollow annular nanoparticles prepared from high-intensity ultrasonic treatment. ACS Nano 16(6):8928–8938. https://doi.org/10.1021/acsnano.1c11167

    Article  CAS  PubMed  Google Scholar 

  53. Langan Nishiyama (2000) Wada, Sugiyama and Chanzy (2000) Crystal structure and hydrogen-bonding system in cellulose from neutron fiber diffraction. ABSTR PAP AMER CHEM SOC 219:U262–U262. https://doi.org/10.1021/ja0257319

    Article  CAS  Google Scholar 

  54. Li L, Wu R, Guang S, Su X, Xu H (2013) The investigation of the hydrogen bond saturation effect during the dipole–dipole induced azobenzene supramolecular self-assembly. Phys Chem Chem Physics Pccp 15(47):20753–20763. https://doi.org/10.1039/c3cp52864b

    Article  CAS  Google Scholar 

  55. Y. Li, YushangLiu, YangLai, WenchuanHuang, FengOu, AnpingQin, RuiLiu, XiangyangWang, Xu (2018) Ester crosslinking enhanced hydrophilic cellulose nanofibrils aerogel. ACS Sustain Chem Eng 6(9).https://doi.org/10.1021/acssuschemeng.8b02284

Download references

Funding

This work was financially supported by the Natural Science Basic Research Plan in Shaanxi Province of China (2021JQ-537) and Natural Science Foundation of Shaanxi University of Science & Technology.

Author information

Authors and Affiliations

  1. Shaanxi Provincial Key Laboratory of Papermaking Technology and Specialty Paper Development, College of Bioresource Chemical and Materials Engineering, Shaanxi University of Science and Technology, Xi’an, 710021, People’s Republic of China

    Tengfei Zhao, Huaiqin Ma, Yuxi Liu, Zhenjuan Chen, Qingwen Shi & Lulu Ning

Authors
  1. Tengfei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huaiqin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuxi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenjuan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qingwen Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lulu Ning
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Tengfei Zhao: Writing—original draft, Software, Methodology, Data curation. Huaiqin Ma: Writing—review, Supervision, Project administration, Conceptualization. Lulu Ning: Writing—review & editing, Supervision, Project administration All authors contributed to the validation of the manuscript and approved the manuscript.

Corresponding author

Correspondence to Lulu Ning.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 8157 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, T., Ma, H., Liu, Y. et al. Interfacial interactions between spider silk protein and cellulose studied by molecular dynamics simulation. J Mol Model 30, 156 (2024). https://doi.org/10.1007/s00894-024-05945-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00894-024-05945-w

Keywords

Search

Navigation