The molecular mechanisms underlying mussel adhesion

Abstract

Marine mussels are able to firmly affix on various wet surfaces by the overproduction of special mussel foot proteins (mfps). Abundant fundamental studies have been conducted to understand the molecular basis of mussel adhesion, where the catecholic amino acid, l-3,4-dihydroxyphenylalanine (DOPA) has been found to play the major role. These studies continue to inspire the engineering of novel adhesives and coatings with improved underwater performances. Despite the fact that the recent advances of adhesives and coatings inspired by mussel adhesive proteins have been intensively reviewed in literature, the fundamental biochemical and biophysical studies on the origin of the strong and versatile wet adhesion have not been fully covered. In this review, we show how the force measurements at the molecular level by surface force apparatus (SFA) and single molecule atomic force microscopy (AFM) can be used to reveal the direct link between DOPA and the wet adhesion strength of mussel proteins. We highlight a few important technical details that are critical to the successful experimental design. We also summarize many new insights going beyond DOPA adhesion, such as the surface environment and protein sequence dependent synergistic and cooperative binding. We also provide a perspective on a few uncharted but outstanding questions for future studies. A comprehensive understanding on mussel adhesion will be beneficial to the design of novel synthetic wet adhesives for various biomedical applications.

Fig. 1. Mussel adhesion and schematic structure of mussel byssus.

Fig. 2. Force and loading rate ranges of different force measurement approaches. OT represents optical tweezers and its range is estimated from ref. 42–44. Bio-membrane force probe (BFP) is estimated from ref. 45. AFM-based SMFS data are from ref. 46–48 and are estimated by general AFM technical details and typical cantilever mechanical properties. SFA data are from ref. 33, 49 and 50. Tensile stretching data are estimated from ref. 47 and 51–54.

Fig. 3. Illustrative scheme of SFA (a) and two types of SMFS (c) and (e) measurements. (b) is the representative force–distance relationship of SFA measurement, (d) is the representative force–extension curve of single-ligand recognition and (f) is the polymer-based fishing measurement.

Fig. 4. Schematic figures of energy landscape (a) and force–loading rate dependency (b). Applied force can tilt the energy landscape and lower the energy barrier. By fitting force–loading rate relationship, dissociation rate and distance to transition state can be extracted.

Fig. 5. Representative force–extension curve and rupture force histogram from different DOPA surface interaction studies. (a and b) are reproduced from Lee et al. Copyright (2006) National Academy of Sciences, U.S.A. (c and d) are reprinted from Wang et al. Copyright (2008) Wiley. Used with permission from ref. 112 and (e and f) are reprinted with permission from ref. 13. Copyright (2014) American Chemical Society.

Fig. 6. Influence of surface atom arrangement on DOPA adhesion. Schematics of different rutile surface atom arrangements and proposed binding modes of DOPA–surface interactions (a). Rupture force histograms observed from DOPA and different rutile surfaces (b). Copyright (2017) Wiley. Used with permission from ref. 16.

Fig. 7. Force distribution of lysine–DOPA and DOPA lysine dipeptides and the TiO₂ surface (a), and the schematic of the unbinding process of Dopa containing dipeptides (b). Reproduced from ref. 17 with permission from the Royal Society of Chemistry.

Fig. 8. Schematics of SMFS study on catechol–Fe³⁺ complex (a) and force spectroscopy (b). Reprinted with permission from ref. 100. Copyright (2017) American Chemical Society.

Yiran Li

Yi Cao