(311e) Molecular Dynamics Investigation of Biomolecule Adsorption to Graphene and Modified Graphene: Molecular Insights into Biofilm Formation and Adhesion

Despite their prevalence in natural and engineered systems (such as biomedical devices), the exact molecular mechanisms and forces controlling biofilm formation and adhesion are relatively unknown. Moreover, surface engineering of these systems to prevent microbial adhesion and biofilm formation has become a key challenge for both the biomedical and materials/corrosion communities. While most modeling studies to date have focused more on continuum or macroscopic film behavior, investigations at the molecular level are needed, too.

Graphene and graphene derivatives are potential candidates to be used as biofilm inhibiting coatings for metal surfaces due to their potential antibacterial properties.[1-2] Chemical vapor deposition (CVD), an alternative to mechanical exfoliation of graphite, is a promising process for large scalable synthesis of graphene. However, CVD usually results in a number of structural defects and surface impurities. While defect-free graphene growth using CVD is still under investigation and these defects remain largely undesired, studies have shown defective graphene surfaces have distinct properties from the pristine layers. What remains to be known is what effect these surface defects have on biofilm adhesion and formation, since no foundational atomistic-level information is available on whether these defects produce positive or negative surface adsorption characteristics relevant to biofilm adhesion and formation.[3]

Recent work has hypothesized that biofilm formation and adhesion may be related to the adsorption of key, early protein molecules including exopolysaccharides (EPS) to surfaces.[4] Nevertheless, studies related to molecular mechanics of these early protein molecule-surface interaction and adsorptive performance of graphene and graphene derivative surfaces is rather scarce. As a first step towards exploring this hypothesis, we investigate the adsorption behaviors of 20 proteinogenic amino acids (as model compounds for microbes), the building blocks of proteins, on pristine and defect-induced graphene surfaces, along with a functionalized surface group (i.e. -COOH, associated with graphene oxide) using molecular dynamics (MD) simulations. All the simulations were conducted in vacuum and in the presence of explicit water as solvent to deduce the effect of solvation on the adsorption behavior.

Specifically, the molecular dynamics simulations are conducted using the LAMMPS molecular dynamics simulation software package and the Adaptive Intermolecular Reactive Empirical Bond Order (AIREBO) and Assisted Model Building with Energy Refinement (AMBER) potentials.[5]–[7] The adsorption energies and the binding free energies of the amino acids on graphene and defective/graphene-derivative/graphene-modified surfaces are evaluated to assess the effect of surface defects on the adsorption phenomena. The binding free energies are computed using the umbrella sampling technique.[8]

The results of this molecular-level study should aid in developing a larger, fundamental understanding of the interaction, adsorption, and adhesion of proteins and microbes to two-dimensional surfaces, such as found in biomedical device applications.

[1] S. V. Agarwalla et al., “Hydrophobicity of graphene as a driving force for inhibiting biofilm formation of pathogenic bacteria and fungi,” Dent. Mater., vol. 35, no. 3, pp. 403–413, 2019.

[2] M. Cacaci, C. Martini, C. Guarino, R. Torelli, F. Bugli, and M. Sanguinetti, “Graphene oxide coatings as tools to prevent microbial biofilm formation on medical device,” in Advances in Experimental Medicine and Biology, vol. 1282, Springer, 2020, pp. 21–35.

[3] S. P. Singh, S. Ramanan, Y. Kaufman, and C. J. Arnusch, “Laser-Induced Graphene Biofilm Inhibition: Texture Does Matter,” ACS Appl. Nano Mater., vol. 1, no. 4, pp. 1713–1720, 2018.

[4] J. Wang, K. M. Goh, D. R. Salem, and R. K. Sani, “Genome analysis of a thermophilic exopolysaccharide-producing bacterium - Geobacillus sp. WSUCF1,” Sci. Rep., vol. 9, no. 1, pp. 1–12, 2019.

[5] S. Plimpton, “Short-Range Molecular Dynamics,” J. Comput. Phys., vol. 117, no. 6, pp. 1–42, 1997.

[6] E. Darian and P. M. Gannett, “Application of molecular dynamics simulations to spin-labeled oligonucleotides,” J. Biomol. Struct. Dyn., vol. 22, no. 5, pp. 579–593, 2005.

[7] S. J. Stuart, A. B. Tutein, and J. A. Harrison, “A reactive potential for hydrocarbons with intermolecular interactions,” J. Chem. Phys., vol. 112, no. 14, pp. 6472–6486, 2000.

[8] G. M. Torrie and J. P. Valleau, “Nonphysical Sampling Distributions in Monte Carlo Free-Energy Estimation: Umbrella Sampling,” J. Comput. Phys., vol. 23, p. 187, 1977.