(Un)expected Similarity of the Temporary Adhesive Systems of Marine, Brackish, and Freshwater Flatworms

Abstract

Many free-living flatworms have evolved a temporary adhesion system, which allows them to quickly attach to and release from diverse substrates. In the marine Macrostomum lignano, the morphology of the adhesive system and the adhesion-related proteins have been characterised. However, little is known about how temporary adhesion is performed in other aquatic environments. Here, we performed a 3D reconstruction of the M. lignano adhesive organ and compared it to the morphology of five selected Macrostomum, representing two marine, one brackish, and two freshwater species. We compared the protein domains of the two adhesive proteins, as well as an anchor cell-specific intermediate filament. We analysed the gene expression of these proteins by in situ hybridisation and performed functional knockdowns with RNA interference. Remarkably, there are almost no differences in terms of morphology, protein regions, and gene expression based on marine, brackish, and freshwater habitats. This implies that glue components produced by macrostomids are conserved among species, and this set of two-component glue functions from low to high salinity. These findings could contribute to the development of novel reversible biomimetic glues that work in all wet environments and could have applications in drug delivery systems, tissue adhesives, or wound dressings.

Sticking Together an Updated Model for Temporary Adhesion

“…Lectin staining also revealed the presence of ap2 in the footprint (i.e., the material that is left behind upon detachment) of M. lignano. Similar results were obtained in other Macrostomum species, as well as in the proseriate M. ileanae [27,28].…”

“…The large adhesive genes of flatworms identified so far are known to be considerably fragmented in transcriptomes due to the presence of multiple repeat regions and extended sections of low-complexity sequences [26][27][28]. Therefore, we aimed to obtain a genome of T. mediterranea to infer the number of repeats and the nature of the low-complexity regions.…”

“…One particularity in the early-branching flatworm taxon Macrostomorpha is that adhesive and releasing glands share a microvilli collar [23,24]. In Macrostomum, one adhesive cell and one releasing cell will always produce a single adhesive papilla [27], whereas in other flatworm groups, such as Proseriata, Polycladida, Rhabdocoela, and Tricladida, both the adhesive and releasing gland cell necks branch multiple times [23]. In these flatworm taxa, it was reported that the releasing gland cell necks emerge individually from the anchor cell, that they are interspersed between the adhesive papillae, and that they do not have a microvillus collar [23].…”

“…Two large, low-complexity regions flank Mlig-ap1, whereas Mlig-ap2 has a repetitive core that spans over nearly two-thirds of the whole protein [26]. Recently, the adhesive system of six other macrostomid flatworms inhabiting fresh, brackish, or seawater environments were thoroughly described, and a high similarity of adhesive proteins independent of the aquatic environment was reported [27].…”

“…In addition to L-DOPA, which was only described in permanent adhesion, it was shown that other post-translational modifications (PTMs) might also play a role in wet adhesion [13,16,22,26,27,30]. The adhesive protein in macrostomids (Mlig-ap2) is glycosylated [26] and was visualised in the adhesive vesicles using peanut agglutinin lectin (a carbohydrate-binding protein) staining [30].…”