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

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.

Interspecies comparison of sea star adhesive proteins.

Sea stars use adhesive secretions to attach their numerous tube feet strongly and temporarily to diverse surfaces. After detachment of the tube feet, the adhesive material stays bound to the substrate as so-called 'footprints'. In the common sea star species Asterias rubens, the adhesive material has been studied extensively and the first sea star footprint protein (Sfp1) has been characterized. We identified Sfp1-like sequences in 17 additional sea star species, representing different taxa and tube foot morphologies, and analysed the evolutionary conservation of this protein. In A. rubens, we confirmed the expression of 34 footprint proteins in the tube foot adhesive epidermis, with 22 being exclusively expressed in secretory cells of the adhesive epidermis and 12 showing an additional expression in the stem epidermis. The sequences were used for BLAST searches in seven asteroid transcriptomes providing a first insight in the conservation of footprint proteins among sea stars. Our results highlighted a high conservation of the large proteins making up the structural core of the footprints, whereas smaller, potential surface-binding proteins might be more variable among sea star species. This article is part of the theme issue 'Transdisciplinary approaches to the study of adhesion and adhesives in biological systems'.