In the footsteps of sea stars: deciphering the catalogue of proteins involved in underwater temporary adhesion

Abstract

Sea stars adhere strongly but temporarily to underwater substrata via the secretion of a blend of proteins, forming an adhesive footprint that they leave on the surface after detachment. Their tube feet enclose a duo-gland adhesive system comprising two types of adhesive cells, contributing different layers of the footprint and de-adhesive cells. In this study, we characterized the catalogue of sea star footprint proteins (Sfps) in the species Asterias rubens to gain insights in their potential function. We identified 16 Sfps and mapped their expression to type 1 and/or type 2 adhesive cells or to de-adhesive cells by double fluorescent in situ hybridization. Based on their cellular expression pattern and their conserved functional domains, we propose that the identified Sfps serve different functions during attachment, with two Sfps coupling to the surface, six providing cohesive strength and the rest forming a binding matrix. Immunolabelling of footprints with antibodies directed against one protein of each category confirmed these roles. A de-adhesive gland cell-specific astacin-like proteinase presumably weakens the bond between the adhesive material and the tube foot surface during detachment. Overall, we provide a model for temporary adhesion in sea stars, including a comprehensive list of the proteins involved.

Structural and evolutionary insights into astacin metallopeptidases

“…However, pod attachment is apparently not based on suction but on a secreted glue consisting of adhesive matrix proteins that are left on the surface after detachment. The latter is mediated by an astacin MP spanning a CD and a CUB domain (CUB_ASTRU; see Figure 5 ; Supplementary Table S1 ), which is specifically secreted by de-adhesive gland cells and releases the adhesive material from the surface of the tube feet ( Algrain et al, 2022 ).…”

Glycoproteins Involved in Sea Urchin Temporary Adhesion

“…Alpha-tectorin-like proteins can be linked to adhesive footprint cohesion and fibrous meshwork formation (already described for sea urchins adhesive [ 52 ]), by promoting protein multimerization into fibers [ 53 ], given its high cysteine content (known to be involved in strong disulfide bonds) and repetitive EGF-like and vWF domains). Being heavily glycosylated and containing glycan-binding lectin domains, sugar–protein interactions can also be involved in their non-covalent cross-linking with other components of P. lividus adhesive and/or of the disc cuticle [ 20 ].…”

“…The involvement of protease inhibitors (Alpha-macroglobulin-like proteins) in sea urchin adhesion is in accordance with the current accepted enzymatic model [ 4 , 19 , 22 ]. Being reported in other aquatic temporary attaching organisms, such as barnacle cyprids (SIPC), sea stars (Arub-13, Spf-9), limpets (P- vulgata-5) and ascidians larvae (H2Y2X2) [ 4 , 53 , 56 , 57 , 58 ], protease inhibitors would provide control of the proteolytic action of the de-adhesive secretion and/or inactivate microbial proteases to protect the secreted adhesive from microbial degradation. The best-studied Alpha-macroglobulin-like adhesive protein is the settlement-inducing protein complex (SIPC) secreted by barnacle cyprid larvae.…”

The Involvement of Cell-Type-Specific Glycans in Hydra Temporary Adhesion Revealed by a Lectin Screen

“…In other temporarily adhering animals, such as sea stars, the amount of secreted adhesive material varies depending on the surface composition [ 27 ] and the strength and duration of attachment [ 28 ]. In Hydra , no correlation between the thickness of the footprints and attachment time could be determined.…”

“…Nevertheless, the approach has its limitations, as recombinant production via bacteria is restricted to single proteins and fails to reproduce any post-translational modifications of the proteins. The natural sea star adhesive consists of a set of 16 proteins [ 28 ], of which many are glycosylated [ 7 ]. The recombinant proteins, therefore, only represent a fraction of the natural adhesive.…”