The structural and chemical basis of temporary adhesion in the sea star Asterina gibbosa

Abstract

Background: Marine biological adhesives are a promising source of inspiration for biomedical and industrial applications. Nevertheless, natural adhesives and especially temporary adhesion systems are mostly unexplored. Sea stars are able to repeatedly attach and detach their hydraulic tube feet. This ability is based on a duo-gland system and, upon detachment, the adhesive material stays behind on the substrate as a 'footprint'. In recent years, characterization of sea star temporary adhesion has been focussed on the forcipulatid species Asterias rubens. Results: We investigated the temporary adhesion system in the distantly related valvatid species Asterina gibbosa. The morphology of tube feet was described using histological sections, transmission-, and scanning electron microscopy. Ultrastructural investigations revealed two adhesive gland cell types that both form electron-dense secretory granules with a more lucid outer rim and one de-adhesive gland cell type with homogenous granules. The footprints comprised a meshwork on top of a thin layer. This topography was consistently observed using various methods like scanning electron microscopy, 3D confocal interference microscopy, atomic force microscopy, and light microscopy with crystal violet staining. Additionally, we tested 24 commercially available lectins and two antibodies for their ability to label the adhesive epidermis and footprints. Out of 15 lectins labelling structures in the area of the duo-gland adhesive system, only one also labelled footprints indicating the presence of glycoconjugates with α-linked mannose in the secreted material. Conclusion: Despite the distant relationship between the two sea star species, the morphology of tube feet and topography of footprints in A. gibbosa shared many features with the previously described findings in A. rubens. These similarities might be due to the adaptation to a benthic life on rocky intertidal areas. Lectin- and immuno-labelling indicated similarities but also some differences in adhesive composition between the two species. Further research on the temporary adhesive of A. gibbosa will allow the identification of conserved motifs in sea star adhesion and might facilitate the development of biomimetic, reversible glues.

Interspecies comparison of sea star adhesive proteins

“…B 374: 20190195 proteins, however, allows identifying common protein characteristics like amino acid composition and functional domains and thereby facilitates the design of biomimetic glues. In sea stars, comparative studies on the adhesive material have been limited to morphological and immunohistochemical investigations, which hint at some conservation between species [2,9,28,29]. In this study, we used the footprint protein (Sfp) sequences from A. rubens to investigate sequence similarity within asteroid orders.…”

“…However, as the antibodies were directed against a short peptide sequence that varies among species, a negative staining result does not indicate the absence of Sfp1. Indeed, in Asterina gibbosa the antibody showed no immunoreactivity [28], but Sfp1 was identified in the new tube foot-specific transcriptome and its expression within the adhesive glands was confirmed with in situ hybridization (electronic supplementary material, figure S5a). The only two species with a positive Sfp1 beta staining in adhesive secretory granules were M. glacialis and Henricia sp (electronic supplementary material, figure S1).…”

Dynamic biological adhesion: mechanisms for controlling attachment during locomotion

“…However, glues do not have to be permanent, and indeed are also used for locomotion in temporary underwater adhesive systems. For example, flatworms and echinoderms achieve repeated attachment and detachment by the subsequent release of adhesive and de-adhesive secretions, each produced by distinct glands or cells [14,[18][19][20]. Glue-based adhesion and de-adhesion require (i) the secretion of the adhesive, (ii) contact formation, (iii) solidification, (iv) secretion of the release agent, (v) its diffusion into the adhesive, and (vi) reaction with it.…”

Integrative Transcriptome and Proteome Analysis of the Tube Foot and Adhesive Secretions of the Sea Urchin Paracentrotus lividus

“…Adhesive cells can be of one or more types and have long necks ending as cuticular pores in sea stars or tufts of microvillar-like projections in sea urchins, through which the adhesive is delivered to the surface [35]. The three most commonly studied echinoderms in terms of their adhesive organs and footprint composition are the sea stars Asterias rubens and Asterina gibbosa [37][38][39][40][41][42] and the sea urchin Paracentrotus lividus [43][44][45][46]. Figure 1.…”

“…Glycans are also an important component of sea star adhesives. The adhesive footprints of A. rubens contain sialylated proteoglycans and two glycoproteins with galactose, N-acetylgalactosamine, fucose and sialic acid residues [40], whereas in A. gibbosa only α-linked mannose glycans have been detected [41].…”