Abstract
Barnacles adhere by producing a mixture of cement proteins (CPs) that organize into a permanently bonded layer displayed as nanoscale fibers. These cement proteins share no homology with any other marine adhesives, and a common sequence-basis that defines how nanostructures function as adhesives remains undiscovered. Here we demonstrate that a significant unidentified portion of acorn barnacle cement is comprised of low complexity proteins; they are organized into repetitive sequence blocks and found to maintain homology to silk motifs. Proteomic analysis of aggregate bands from PAGE gels reveal an abundance of Gly/Ala/Ser/Thr repeats exemplified by a prominent, previously unidentified, 43 kDa protein in the solubilized adhesive. Low complexity regions found throughout the cement proteome, as well as multiple lysyl oxidases and peroxidases, establish homology with silk-associated materials such as fibroin, silk gum sericin, and pyriform spidroins from spider silk. Distinct primary structures defined by homologous domains shed light on how barnacles use low complexity in nanofibers to enable adhesion, and serves as a starting point for unraveling the molecular architecture of a robust and unique class of adhesive nanostructures.
Highlights
Natural materials have remarkable functional properties and ambient processability: threads with high strength, glues that cure underwater, and ceramics that resist fracture
Integrated proteomic and transcriptomic analysis reveals that nanofibrillar cement in barnacle adhesive is comprised primarily of a new and unique family of polar proteins
Glycine/Serine rich Cement Proteins (GSrCP) were not found in translated mRNA libraries assembled from other regions of the organism, or in MS/MS analysis of fluid collected from canals that line the side plates
Summary
Natural materials have remarkable functional properties and ambient processability: threads with high strength, glues that cure underwater, and ceramics that resist fracture. Over a 20 year period, five protein sequences have been identified through the use of aqueous denaturants such as guanidine hydrochloride, formic acid, and urea[17,18,19] These treatments have solubilized a fraction of barnacle cement, though the inability to target the primary interactions between cement proteins remains a significant roadblock. Extensive studies of mRNA and protein expression in barnacles have provided systemic insight into metamorphosis, adult development and molting[31,32,33,34] This has been enabled by the development of high throughput RNA sequencing (RNA-seq) as well as tandem mass spectrometry methods that together create proteomic databases directly from complex materials[35]. Without direct proteomic sequencing of solubilized cement, insight into nanostructure composition and the relationship of components with themselves or other adhesive materials remains a challenge
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