Chapter 1
Bio-inspired Coatings and Adhesives

Saurabh Das1,2,3 and B. Kollbe Ahn1,3*

1Marine Science Institute, University of California, Santa Barbara, CA 93106, USA

2Chemical Engineering, University of California, Santa Barbara, CA 93106, USA

3Materials Research Science and Engineering Center, University of California, Santa Barbara, CA 93106, USA

*Corresponding author: kollbe.ahn@lifesci.ucsb.edu

Abstract

Biological organisms such as marine mussels have attracted attention as a paradigm of strong and versatile adhesion to hard surfaces under the severe chemical and physical environments of the wave-swept shores. Recent studies to understand the molecular mechanisms and mechanochemical aspects of mussel foot protein adhesion to different substrates have inspired the development of a variety of underwater adhesives, strain-resistant materials, hydrogels, self-healing polymers, and surfactants for tissue repair, drug delivery, anti-fouling coatings, and medical adhesives applications. In this chapter, we start to systematically discuss the physicochemical process at the molecular level during the attachment of mussel plaque to a substrate followed by the role of different amino acid residues in the attachment process. We then provide fundamental insights into the molecular architecture-function relationship for synthetic bio-inspired adhesives as well as begin to develop design principles for bio-inspired wet adhesives. This is followed by a thorough review of the recent development in mussel-inspired underwater polymer adhesive coatings and surfactant nano-adhesives that emphasizes the importance of the balance between electrostatic and hydrophobic interactions for wet adhesion and coacervation in addition to catecholic interactions, e.g., oxidative cross-linking, metal coordination, and intermolecular hydrogen bonding. We also shed light on intermolecular hydrogen bonding for surface-initiated underwater self-healing of polymers and metal-mediated cross-linking inspired from the mussel threads that provide sacrificial and reversible bonds at interfaces for strain-resistant materials.

Keywords: Mussel, wet, underwater, adhesives, coatings

1.1 Introduction

Nature has developed surprisingly elegant and diversified adaptations for the survival of the fittest organisms by a smart control of the interfacial forces and regulating surface interactions with the surroundings. For instance, geckos can cling and run with impeccable dexterity on most surfaces regardless of its roughness by controlling the frictional adhesion [1, 2] between its hierarchical fibrillar structures on the footpad and the surface. They avoid slip [3] during sticking and shearing of the nanosized spatula on a surface and employ van der Waals' forces [4] to adhere to dry surfaces. Similarly, tree frogs that reside in the arboreal habitat of the wet rainforests take advantage of the capillary and viscous forces to prevent it from falling while running on surfaces [5, 6]. Currently, researchers in the wet adhesion community are spearheaded to solve the engineering challenge of wet underwater adhesion through mimicking techniques employed by the marine organisms such as barnacles [7, 8], pearl oysters [9, 10], minicollagens from sea anemones [11], sandcastle worms [12, 13], and the marine mussels [14, 15].

Harsh intertidal oceanic waves are no match for the mighty mussel that produces strong, flexible threads and cling to the surfaces of rocks, piers, and boats and even to other mussels without getting washed by the impact of water. This extraordinary ability of the mussels to adhere to any surface underwater has been baffling researchers for the past few decades. The adhesion mechanism used by the marine mussels has been extensively explored recently, and efforts have been made to develop coatings and adhesives for a variety of applications ranging from dental adhesives [16], self-assembled bilayer nano-adhesives [17], antifouling surfaces [18], self-healing polymers [19], drug delivery chaperons [20], medical glues [21], etc. Understanding the technique used by the mussels to prepare the surface for adhesion and the molecular mechanism underpinning the adhesive strength of the mussel glue (i.e., the mussel foot proteins or mfps) is fundamental to design synthetic mimics of the biological system.

1.2 The Interfacial Biochemistry of a Mussel Adhesive

Marine mussels are experts at 'wet' adhesion, achieving strong and durable attachment to a variety of surfaces in their marine habitat. Adhesion is mediated by a byssus, essentially a bundle of leathery threads that emerge from living mussel tissue at one end and tipped by flat adhesive plaques at the other (Figure 1.1). The byssal plaques consist of a complex array of proteins (mostlysix different mussel foot proteins, mfps 1-6), each of which has a distinct localization and function in the structure, but all share the unusual amino acid 3,4-dihydroxyphenylalanine (Dopa), a post-translational modification from tyrosine (Tyr or Y), that features prominently in mfps, ranging from less than 5 mol% in mfp-4 to 30 mol% in mfp-5 [24-29]. Mussels use its foot to make a snug contact with a target surface prior to depositing adhesive mfps in a fashion resembling injection molding [30]. The dimpled distal depression of the foot is positioned over a surface like an inverted rubber cup and compressed, thereby pushing out bulk water. Mfps are then secreted into the remaining gap from 8 to 10 pores in the depression ceiling [31].

Figure 1.1 Dr. Nadine Martinez (former graduate student at the University of California Santa Barbara, currently postdoc at the Stanford School of Medicines), picking up mussel from the wave-swept beach shore at UCSB campus point during low tide (Left, Photo credits: Saurabh Das). A mussel secured to a mineral surface (Right inset). Adhesive mfps such as mfp-3 (blue circles) and mfp-5 (green circles) binds the plaque to a mineral surface. In mussel byssal threads, collagens known as preCOLs mediate the transfer of load between the mussel plaque and the thread [22]. PreCOLs come within a few nm of the mica surface and thus may bind directly to adhesive mfps such as mfp-3 and mfp-5. The preCOLs are protected by a coating protein, mfp-1, that can accommodate high strains while simultaneously contributing to its disparate stiffness. (Adapted from Thesis [23]: Das, S. Bio-Inspired Adhesion, Friction and Lubrication, University of California, Santa Barbara, 2014, 226 pages; 3682889.)

Strong and durable adhesion is achieved despite the surrounding seawater at pH 8.2, high salt and saturating levels of dissolved O2. The interfacial pH at which mussels buffer the local environment during mfp deposition was determined using a pH-sensitive surface (e.g., mica functionalized with a fluorescent bilayer) to range from 2.2 to 3.3, which is well below the seawater pH of 8 [14]. The mussel foot significantly acidifies the interface during initial protein deposition (Figure 1.2). The role of acidification isto retard the oxidation of Dopa residues in the mfps for the formation of hydrogen bonds, metal-catechol coordination, or cation-p interactions with the surface to secure the proteins/plaque to the substrate. Deposition of adhesive proteins at acidic pH has important implications for mussel-inspired technology. The acidic pH allows delivery of the mfps to a surface as complex coacervate fluids; together with antioxidants [32], stabilizes the catecholic residue in the protein enabling the formation of electrostatic bonds with a mineral surface or coordination bonds with the surface oxides; favors the formation of cationic functionalities, e.g., Lys, Arg, and His for long-range attraction to electronegative surfaces. The acidic pH in combination with seawater (pH 8.2) serves as a switch for initiating protein insolubility, quinone-based cross-linking and catechol-mediated metal chelation (Figure 1.3).

Figure 1.2 Fluorescent images and intensities of the plaque substrate interface during plaque formation by juvenile mussels (<10 mm). Transmitted light images taken at t = 0 and t = 11.5 min, respectively, of an Oregon Green DHPE/DMPC-labeled mica surface during foot contact (a) and following foot disengagement (b) from the new plaques. Corresponding fluorescence images are in (c) and (d). Distal depression of the foot is highlighted by a red circle (A = 2.7 × 104 µm2, diameter ~209 µm). (e) Change in normalized fluorescence intensity (I) after disengagement of foot from plaque and direct equilibration with seawater. (f) Change in normalized fluorescent intensity (right axis) and pH (left axis) during actual mussel foot-surface contacts (shaded gray area) which typically lasted =180 s in juvenile mussels. This figure has been adapted from Ref. [14].

Figure 1.3 Mussels adhesive plaque formation on a pH-sensitive mica surface depicting chemistry under reducing (acidic pH) and oxidizing (neutral to slightly alkaline pH) conditions. (a) Mussel Mytilus californianus with extended foot and a single completed plaque and thread. (b) Foot contact with a mica surface evicts seawater from the distal depression and lowers the pH to ~2.2. (c) The foot disengages from the surface, and a plaque is deposited. The uncross-linked proteins at low pH interact with the...