A mechanism for temporary bioadhesion

Julia Wunderer,Peter Ladurner,Michael W Hess,Robert Pjeta,Philip Bertemes,Willi Salvenmoser,Birgit Lengerer,Herbert Lindner,Leopold Kremser,Thomas Ederth,David Stock

doi:10.1073/pnas.1814230116

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.

Highlights

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
Our findings provide a better understanding of an effective temporary adhesion system with great biomimetic potential
We have identified two large adhesive proteins, M. lignano adhesion protein 1 (Mlig-ap1) and Mlig-ap2, comprising 5,407 and 14,794 amino acids, respectively

Summary

Introduction

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. A small negatively charged molecule is secreted that interferes with Mlig-ap, inducing detachment These findings are of relevance for fundamental adhesion science and efforts to mitigate biofouling. The secreted adhesive material stays permanently attached to the surface as so-called footprints Such systems are found in echinoderms [7, 11] and flatworms [12,13,14]. We showed that negatively charged sugars were able to inhibit the adhesion, while positively charged molecules interfered with the natural detachment of the flatworm. These results were incorporated into a model for the attachment and release of M. lignano. 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

Methods

Results

Conclusion