Interaction of graphene oxide with tannic acid: computational modeling and toxicity mitigation in C. elegans

Abstract

Graphene oxide (GO) undergoes multiple transformations when introduced to biological and environmental media. GO surface favors the adsorption of biomolecules through different types of interaction mechanisms, modulating the biological effects of the material. In this study, we investigated the interaction of GO with tannic acid (TA) and its consequences for GO toxicity. We focused on understanding how TA interacts with GO, its impact on the material surface chemistry, colloidal stability, as well as, toxicity and biodistribution using the Caenorhabditis elegans model. Employing computational modeling, including reactive classical molecular dynamics and ab initio calculations, we reveal that TA preferentially binds to the most reactive sites on GO surfaces via the oxygen-containing groups or the carbon matrix; van der Waals interaction forces dominate the binding energy. TA exhibits a dose-dependent mitigating effect on the toxicity of GO, which can be attributed not only to the surface interactions between the molecule and the material but also to the inherent biological properties of TA in C. elegans. Our findings contribute to a deeper understanding of GO's environmental behavior and toxicity and highlight the potential of tannic acid for the synthesis and surface functionalization of graphene-based nanomaterials, offering insights into safer nanotechnology development.

Keywords: biodistribution; density functional theory; ecotoxicity; molecular dynamics; surface interactions; toxicity mitigation.

Figure 1

Characterization of the GO and TA interaction system. AFM images of (a) GO and (b) GO incubated with TA (10 mg·L⁻¹). The height profile plots on the right present the topology of the marked regions of each sample image.

Figure 2

Characterization of GO and TA system. a) FTIR showing absorption signals related to –OH strength band, GO’s fingerprint region with 1734(1), 1625(2), 1390(3), 1230(4), and 1068(5) cm⁻¹ bands, and TA-related bands at 1704(6), 1600(7), 1310(8), and 1180(9) cm⁻¹; b) Raman spectra normalized by intensity of G band; High-resolution C 1s XPS analysis of c) GO and d) GO with TA (10 mg·L⁻¹) showing the peaks of carbon sp²+sp³ and oxygenated carbon bonds C–O and C=O.

Figure 3

Snapshot of TA on the GO surface obtained from NPT MD at 300 K, parameterized with the ReaxFF reactive force field. The molecular structure view was generated with the VMD software developed with NIH support by the Theoretical and Computational Biophysics group at the Beckman Institute, University of Illinois at Urbana-Champaign (http://www.ks.uiuc.edu/) [48]. This content is not subject to CC BY 4.0.

Figure 4

Reactive sites of GO (a) before and (b) after NPT dynamics in aqueous environment. Fukui functions f⁺ in yellow (positive) and blue (negative), f⁻ in purple (positive) and green (negative). Isosurface of 1 × 10⁻³ e/ų. The molecular structure view was generated with the VMD software developed with NIH support by the Theoretical and Computational Biophysics group at the Beckman Institute, University of Illinois at Urbana-Champaign (http://www.ks.uiuc.edu/) [48]. This content is not subject to CC BY 4.0.

Figure 5

Adsorption energy of TA on GO surfaces with different oxidation degree. The error bars indicate the standard error of the mean from up to ten configurations.

Figure 6

Effects of GO in presence or absence of TA on C. elegans’ survival. α and β indicate survival rates significantly different from the control (100% of survival) with p ≤ 0.05 (one-way ANOVA). *** and ** indicate difference in the treatments with p ≤ 0.001 and p ≤ 0.05 (two-way ANOVA), respectively. The error bars are calculated from 16 to 18 data points on survival.

Figure 7

G-band intensity depth profiles (from −30 to 120 μm) used to monitor biodistribution of GO, and GO with 1 and 10 mg·L⁻¹ of TA in different tissues of nematodes.