Neutral glycans from sandfish skin can reduce friction of polymers

Abstract

The lizardScincus scincus, also known as sandfish, can move through aeolian desert sand in a swimming-like manner. A prerequisite for this ability is a special integument, i.e. scales with a very low friction for sand and a high abrasion resistance. Glycans in the scales are causally related to the low friction. Here, we analysed the glycans and found that neutral glycans with five to nine mannose residues are important. If these glycans were covalently bound to acrylic polymers like poly(methyl methacrylate) or acrylic car coatings at a density of approximately one molecule per 4 nm², friction for and adhesion of sand particles could be reduced to levels close to those observed with sandfish scales. This was also found true, if the glycans were isolated from sources other than sandfish scales like plants such as almonds or mistletoe. We speculate that these neutral glycans act as low density spacers separating sand particles from the dense scales thereby reducing van der Waals forces.

Keywords: Scincus; integument; mannose; mass spectroscopy; sand swimming.

Figure 1.

Comparison of the appearance of the sandfish Scincus scincus and the Berber skink Eumeces schneideri. (a) An adult specimen of S. scincus photographed during a short stay on the sand surface in a terrarium. As can be seen clearly, the scales are not scratched as they reflect brightly and no sand adheres onto the surface, although the animal just rose up from the sand. (b) The genetically closely related but not sand swimming E. schneideri is shown for comparison. These lizards tend to dig in the sandy ground, but do not actively bury. Clearly, ground particles adhere onto the scales, especially at the snout and the legs, the body parts which are mainly used to dig.

Figure 2.

The proposed mechanism of PMMA glycosylation. In our method, first the amino-linker hexamethylene diamine is attached to the acrylic surface by attacking the methoxy group, creating a free primary amine on the surface. In the second step, a glycan is linked to the amine through a reductive amination reaction. For this to work, the first GlcNAc has to undergo a ring-opening, thus creating a free aldehyde group, which can react with the free primary amine on the acrylic surface.

Figure 3.

Friction measurements of sandfish epidermis and PMMA. Friction angle is shown on the left vertical axis for dark columns, while the calculated friction coefficient is shown on the right for bright columns. Ten independent measurements were performed for every sample. While there is a small but significant (*, confidence level α = 0.9, two sided unpaired t-test) reduction of friction due to activation of PMMA (PMMA-NH₂) in comparison to untreated PMMA (PMMA), the further friction reduction due to glycosylation of PMMA (PMMA SF Ngly) is highly significant (**, α = 0.99). However, the level of the native sandfish scales (SF skin) is not fully reached using the current protocol.

Figure 4.

AFM adhesion force measurements of PMMA with different levels of glycosylation with neutral N-glycans. Typical force–distance curves are shown as insets for unglycosylated and ‘fully’ glycosylated PMMA. The adhesive force can be seen as height of the triangular snap in the retrace curve (fair curve). Clearly, a sigmoidal decrease of the adhesive forces can be observed with increasing glycosylation level. For comparison, the values of native sandfish skin and PMMA-NH₂ are shown. Each data point represents the average unbinding force from 10 force–distance curves. Error bars depict the standard deviation.

Figure 5.

MALDI time-of-flight mass spectrometric analysis of S. scincus skin lysate N-glycans. Based on the masses and mass increments according to hexoses (204 m/z) and hexosamines (245 m/z), the inserted neutral glycans could be identified at the given m/z-values. Circles indicate mannose residues (Man), squares are hexosamines (GlcNAc). A semi-quantitative evaluation was made as follows: ++, major signal (more than 25% of the base peak intensity in the mass range m/z 1000–5000); +, significant signal with 5–25% of base peak intensity.

Figure 6.

Friction measurements of modified PMMA with all sandfish glycans and with pure mannose 5 N-glycan (H5N2). The friction angles were measured 10 times on every sample. No significant difference between H5N2-coated PMMA and PMMA coated with all sandfish glycans can be detected (n.s., two sided t-test, α = 0.99) while there is a significant (**) reduction when compared to uncoated PMMA.

Figure 7.

Sand adhesion and friction on native and glycosylated acrylic lacquer (brand name GW34). (a) A coated (GW34 + SFgly) and an untreated (GW34) sample were placed side by side on an inclined plane and completely covered with sand. The inclination was gradually increased until sand began to slide off the coated plate. The photograph was taken at an inclination of approximately 30°. (b) Direct comparison of friction angle and friction coefficient for native GW34 lacquer and glycosylated GW34. A friction reduction of approximately 40% could be achieved.

Figure 8.

A three-dimensional model of a M5 (H5N2) glycan in a watery medium. The structure was obtained from GLYCAM database. All the atoms are labelled according to their nature. All the sugars contain carbon (grey), oxygen (red) and hydrogen (white) atoms, the GlcNAcs also contain nitrogen (blue). The cuboid around the molecule has dimensions of 2.25×1.65×1.24 nm.