A mechanism for temporary bioadhesion

Significance

Synthetic adhesives are widely used in our daily lives, in medicine and industry. These man-made glues contain toxic or carcinogenic components. In contrast, biological adhesives produced by animals and plants are nontoxic and tissue-compatible, and are able to function under wet conditions. However, little is known about the mechanisms underlying biological adhesives. We characterized adhesion and release in our model system Macrostomum lignano. We used a state-of-the-art toolbox to identify the involved adhesive and release molecules. We aim for understanding the fundamental mechanisms that mediate adhesion and release in flatworms, with the future goal of generating a flatworm-derived biomimetic glue that can be applied in biomedicine and industry.

Abstract

The flatworm Macrostomum lignano features a duo-gland adhesive system that allows it to repeatedly attach to and release from substrates in seawater within a minute. However, little is known about the molecules involved in this temporary adhesion. In this study, we show that the attachment of M. lignano relies on the secretion of two large adhesive proteins, M. lignano adhesion protein 1 (Mlig-ap1) and Mlig-ap2. We revealed that both proteins are expressed in the adhesive gland cells and that their distribution within the adhesive footprints was spatially restricted. RNA interference knockdown experiments demonstrated the essential function of these two proteins in flatworm adhesion. Negatively charged modified sugars in the surrounding water inhibited flatworm attachment, while positively charged molecules impeded detachment. In addition, we found that M. lignano could not adhere to strongly hydrated surfaces. We propose an attachment–release model where Mlig-ap2 attaches to the substrate and Mlig-ap1 exhibits a cohesive function. A small negatively charged molecule is secreted that interferes with Mlig-ap1, inducing detachment. These findings are of relevance for fundamental adhesion science and efforts to mitigate biofouling. Further, this model of flatworm temporary adhesion may serve as the starting point for the development of synthetic reversible adhesion systems for medicinal and industrial applications.