The adsorption of xyloglucan on cellulose: effects of explicit water and side chain variation
Graphical abstract
Introduction
The plant cell wall is a dynamic biocomposite material, comprised of load-bearing para-crystalline cellulose fibrils embedded in a matrix of cross-linking glycans, (glyco)proteins, and polyphenolics, which undergoes continuous change during tissue differentiation and plant growth.1 Yet, while plant cell wall models continue to be further refined in the light of ongoing ultra-structural analysis, little is presently known about the precise nature of the molecular interactions between cell wall components. This is largely due to a paucity of experimental methods for high-resolution (atomic-level) structural analysis of poorly crystalline solid materials, as typified by the hydrogelatinous plant cell wall.2
Contemporary models of the primary cell wall of dicots and diverse monocots suggest that the non-covalent network formed by insoluble cellulose (β-(1→4)-glucan) chains and the non-crystalline polysaccharide xyloglucan (XG) is a central contributor to wall strength and extensibility.3, 4, 5, 6 XG is a complex branched polysaccharide consisting of a cellulose-like β-(1→4)-glucan main chain regularly substituted with branching α-(1→6) xylosyl residues. Branching is both extensive and highly regular, with xylose substitution at 50–75% of the glucosyl units, depending on the source.7, 8 In XGs typical of many dicots, the repeating motif is based on the XXXG heptasaccharide, where G represents an unbranched Glcp-(1→4) unit and X represents α-d-Xylp-(1→6)-β-d-Glcp-(1→4). Further galactosylation and fucosylation give rise to other common oligosaccharide units such as XXLG and XXFG, where L represents β-d-Galp(1→2)-α-d-Xylp-(1→6)-β-d-Glcp-(1→4) and F represents α-l-Fucp-(1→2)-β-d-Galp-(1→2)-α-d-Xylp-(1→6)-β-d-Glcp-(1→4).9 XG branching affects the solution properties of this family of polysaccharides and is likewise a determinant of the affinity of XGs for cellulose (reviewed in Ref. 10). Elucidating how the diversity of branching patterns affects the cellulose–XG interaction is thus central to improving our understanding of the ultra-structural organization and function of the plant cell wall, which can further inform the use of XG in biomimetic cellulose modification applications.10, 11, 12, 13, 14
Despite a significant number of experimental studies both in vivo15, 16, 17, 18, 19, 20, 21 and in vitro,22, 23, 24, 25, 26 the specific roles of the backbone and various side chain residues in the XG–cellulose interaction remain a subject of debate, essentially due to the structural and morphological complexity of the system and a lack of direct visualization methods. In this regard, computer simulations provide a powerful opportunity to model the adsorption behavior of molecules at interfaces and for exploring atomic-level interpretation of the experimental data.27, 28 A prominent advantage of in silico studies is that the polysaccharide composition can be systematically varied in a model of defined (typically reduced) complexity, thus enabling a more precise determination of the influence of the side chain pattern. Nonetheless, theoretical studies of the XG–cellulose assembly are still rare.22, 29, 30, 31
Due to the compositional similarity between the XG backbone and the cellulose, it has long been suggested that the XG–cellulose interaction may involve alignment of the polysaccharide chains.32 Indeed, early molecular modeling supported this hypothesis, although studies have differed on whether interchain association is mediated by Glc–Glc ring stacking interactions or side-on hydrogen bonds (e.g., Refs. 22, 29, 31, reviewed in Ref. 10). However, a contemporary molecular dynamics (MD) analysis by Hanus and Mazeau has seriously questioned the necessity of parallel chain alignment in the XG–cellulose interaction.30 Rather, XXXG, XXLG, and XXFG oligosaccharides, as well as longer (XXFG)n oligomers, were observed to bind with parallel, antiparallel, and perpendicular orientations to all five unique crystal faces of cellulose Iβ with similar binding energies.
One potential concern with the landmark work of Hanus and Mazeau is that the binding simulations were performed in vacuo, that is, in the absence of solvating water molecules. While on one hand the conformations of both cellulose and XG are known to be regulated by water,33, 34, 35, 36, 37, 38 the existence of highly structured water layers at the cellulose Iβ–water interface has also been indicated.33 Thus, in the present study we have re-examined the XG–cellulose Iβ interaction in the presence of explicit water molecules using MD simulations with NPT ensembles at physiological normal temperature and pressure. Because most of the cellulose fibril surface exposes the hydrophilic sides of the glucose monomers to solution, the cellulose Iβ 1–10 surface was chosen for the study of XG adsorption in water. Three XG oligosaccharides, based on a nine glucose residue backbones (to minimize chain-end effects) and differing in one single side chain (Fig. 1), were selected and their interactions with the cellulose Iβ 1–10 surface were modeled to examine the impact of XG side chain variation on the molecular structure of the complex and energetic properties. Additionally, steered molecular dynamics (SMD) simulations were employed to gain further insight into the binding affinity of the cellulose surface to XGs.
Section snippets
Computational details
All simulations were performed with the Gromacs 4.0 code.39, 40 Throughout the calculation, the potential function takes the following form:where the reference bond length and bond angle are denoted by r0 and θ0, kr, kθ, and υn are force constants. n is the multiplicity and γ is the phase angle for the torsional angle parameters. ε and σ represent the non-bonded Lennard–Jones parameters and q is the
Structural dynamics and energetic dynamics: criteria for the equilibration state
Two criteria were applied to judge if the equilibration of the adsorption has reached, that is, the structural criterion of root mean square deviation (RMSD) of XG; and the energetic criterion of total instantaneous interaction energy between XG and cellulose 1–10 surface Eint(t) defined as:
In (Eq. 5), Eint(t) stands for the total instantaneous interaction between the XG and cellulose at time t during the MD simulation. EXG:cellulose(t) represents
Conclusion
We have, by means of atomistic MD simulations, investigated the adsorption properties of three XG fragments, namely GXXXGXXXG, GXXLGXXXG, and GXXFGXXXG, on the cellulose Iβ 1–10 surface in an aqueous environment, with a particular focus on explicit water in the theoretical model and effects of the side chain variation on adsorption. Our results are consistent with the results of Hanus et al.,30 in which the XG–cellulose interaction was modeled in vacuo, in the following aspects: the parallel
Acknowledgments
This work is supported by a grant from the Swedish National Infrastructure for Computing (SNIC) for the project ‘Multiphysics Modeling of Molecular Materials’, SNIC 022/09-25. H.B. acknowledges funding from the Formas via CarboMat—The KTH Advanced Carbohydrate Materials Consortium, a Formas Strong Research Environment.
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2021, Journal of Colloid and Interface ScienceCitation Excerpt :The value of ΔG at room temperature is −12.8 kJ mol−1 AGU-1 for the native surface, and −3.8 kJ mol−1 AGU-1 for the charged surface. This is in good agreement with the simulated free energies reported by Zhang et al. [26], who obtained ΔG between −14.2 to −15.9 kJ mol−1 AGU-1 using the same force field, but different chemical structure. Another interesting observation for the case of native cellulose is that the curve levels off at higher T, which means that the entropy term trends to zero.