Beneficial characteristics of mechanically functional amyloid fibrils evolutionarily preserved in natural adhesives

Abstract

While biological systems are notorious for their complexity, nature sometimes displays mechanisms that are elegant in their simplicity. We have recently identified such a mechanism at work to enhance the mechanical properties of certain natural adhesives. The mechanism is simple because it utilizes a non-specific protein folding and subsequent aggregation process, now thought to be generic for any polypeptide under appropriate conditions. This non-specific folding forms proteinaceous crossed β-sheet amyloid fibrils, which are usually associated with neurodegenerative diseases. Here we show evidence for the beneficial mechanical characteristics of these fibrils discovered in natural adhesives. We suggest that amyloid protein quaternary structures should be considered as a possible generic mechanism for mechanical strength in a range of natural adhesives and other natural materials due to their many beneficial mechanical features and apparent ease of self-assembly.

Atomic force microscopy of the morphology and mechanical behaviour of barnacle cyprid footprint proteins at the nanoscale

“…Consequently, many naturally occurring bioadhesives are unusually tough by synthetic adhesive standards (Groshong 2007). In fact, sacrificial bonds are abundant in nature and can be found in many biomaterials such as bone (Smith et al 1999;Fantner et al 2005), spider silk (Becker et al 2003), natural adhesives from algae (Callow et al 2000;Mostaert et al 2006;Mostaert & Jarvis 2007), diatom mucilage (Higgins et al 2003;Dugdale et al 2005Dugdale et al , 2006a and adult barnacle cement (Sun et al 2004). In this paper, the morphology and nanomechanical properties of cyprid footprints were investigated with AFM.…”

Nanomechanics of Amyloid Materials Studied by Atomic Force Microscopy

“…This was achieved in the AFM manipulation of amyloid fibrils formed from an 11 amino acid peptide segments of transthyratin, TTR Mostaert & Jarvis, 2007). When the force spectroscopy was conducted on TTR fibrils, similar plateaus were observed, corresponding to the peeling off of -sheets from the fibrils; in addition, force curves with sawtooth pattern were also captured (Figure 7), which were attributed to the successive unraveling of the peptide molecules from the fibril bulk.…”

Functional Amyloid

“…This sawtooth response has a much smaller persistence length than on the blue retraction part of the curve because in this case the ß-sheet is being unravelled as it is pushed into the adhesive matrix (in parallel with the additional stiffness of the adhesive matrix). Amyloid fibrils also readily self-assemble, thus constituting a self-healing material [9].Using a combination of AFM and complementary techniques, we have now identified amyloid structures in the permanent adhesive of five species of algae and one temporary adhesive from an invertebrate organism, leading us to postulate that physiological amyloid may occur far more commonly in nature than previously thought. To a large extent it may have remained undetected due to its lack of dependence on amino acid sequence and the difficulties associated with analyzing the composition of amyloid fibrils that are insoluble and resistant to proteolysis.…”

“…Additional beneficial mechanical characteristics of amyloid arise due to the high degree of rotational symmetry of the fibrils. This means that any force applied tangential to the direction of the fibril will have the same beneficial unfolding characteristics [9]. An example of this can be observed on the red approach curve in figure 4.…”

“…It is apparent from our work on amyloid-like fibrils that there exist qualitative similarities and quantitative differences between different fibrils where the maximum force and number of sawtooth peaks can vary considerably. However, force-extension curves often exhibit either sawtooth or plateau force responses under a tensile load [7].There has been considerable interest in the mechanical properties of amyloid fibrils [8] since the implication of the amyloid fold in spider silk, but our recent work provides the first experimental evidence explaining why this structure has superior mechanical characteristics based on "hidden length" and "sacrificial bonds" [5,7,9]. Additional beneficial mechanical characteristics of amyloid arise due to the high degree of rotational symmetry of the fibrils.…”