Molecular insights into the powerful mucus-based adhesion of limpets ( Patella vulgata L.)

Abstract

Limpets ( Patella vulgata L.) are renowned for their powerful attachments to rocks on wave-swept seashores. Unlike adult barnacles and mussels, limpets do not adhere permanently; instead, they repeatedly transition between long-term adhesion and locomotive adhesion depending on the tide. Recent studies on the adhesive secretions (bio-adhesives) of marine invertebrates have expanded our knowledge on the composition and function of temporary and permanent bio-adhesives. In comparison, our understanding of the limpets' transitory adhesion remains limited. In this study, we demonstrate that suction is not the primary attachment mechanism in P. vulgata ; rather, they secrete specialized pedal mucus for glue-like adhesion. Through combined transcriptomics and proteomics, we identified 171 protein sequences from the pedal mucus. Several of these proteins contain conserved domains found in temporary bio-adhesives from sea stars, sea urchins, marine flatworms and sea anemones. Many of these proteins share homology with fibrous gel-forming glycoproteins, including fibrillin, hemolectin and SCO-spondin. Moreover, proteins with potential protein- and glycan-degrading domains could have an immune defence role or assist degrading adhesive mucus to facilitate the transition from stationary to locomotive states. We also discovered glycosylation patterns unique to the pedal mucus, indicating that specific sugars may be involved in transitory adhesion. Our findings elucidate the mechanisms underlying P. vulgata adhesion and provide opportunities for future studies on bio-adhesives that form strong attachments and resist degradation until necessary for locomotion.

Omics‐based molecular analyses of adhesion by aquatic invertebrates

“…Cnidarians do not possess brains, however they do produce abundant glycoproteins and, with further analysis of the literature, DMBT1 was found to encode a glycoprotein of unknown function in humans (Madsen, Mollenhauer & Holmskov, 2010). Interestingly, a protein identified in limpet mucus, P-vulgata_10, was also annotated as DMBT1 (Kang et al, 2020). Yet, the three proteins are only superficially similar (Fig.…”

“…7). For example, the putative cohesion proteins Mlig-ap1 (flatworm), Sfp1 (sea star) and P-vulgata_1 (limpet) all contain vWD, EGF, and lectin-binding domains, which are known to mediate protein-protein and proteincarbohydrate interactions (Hennebert et al, 2014;Wunderer et al, 2019;Kang et al, 2020). Conserved blocks of different domains might be indicative of common evolutionary origin.…”

“…The surface-binding adhesive protein Mlig-ap2 shares many features of the glycoprotein SCO-spondin, including the vWD-C8-TIL motif, lowdensity lipoprotein receptor (LDL) domains and TSP-1 repeats (Wunderer et al, 2019). Two separate proteins (P-vul-gata_3 and 6), resembling respectively the N-and C-terminal parts of Mlig-ap2, have also been identified in limpets (Kang et al, 2020). A protein with comparable TSP-1 repeats was detected in tunicates (Li et al, 2019).…”

“…It was proposed that SIPC derived from a duplication of an ancestral alpha-2-macroglobulin and was functionally adapted for its role as a settlement cue and potential adhesive (Dreanno et al, 2006;Petrone et al, 2015). In recent years, proteins with similar domain structures have been identified in the adhesive secretions of diverse taxa, including echinoderms Asterias rubens (Hennebert et al, 2015a;Lengerer et al, 2019) and Paracentrotus lividus (Pjeta et al, 2020), the limpet Patella vulgata (Kang et al, 2020) and the tunicate Ciona robusta (Li et al, 2019) (Fig. 7).…”

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“…They live on seashores and withstand tidal waves, wind and predators by strong adhesion from their pedal sole (adhesion tenacity between 0.1 and up to 1.1 MPa). [ 99 ] In contrast to mussels, limpids secrete different glue depending on their purpose: locomotion or stationary attachment. It was found that the differences between both types of mucus are mostly derived by larger protein and carbohydrate content for the stationary mucus.…”