A strong quick-release biointerface in mussels mediated by serotonergic cilia-based adhesion

Abstract

The mussel byssus stem provides a strong and compact mechanically mismatched biointerface between living tissue and a nonliving biopolymer. Yet, in a poorly understood process, mussels can simply jettison their entire byssus, rebuilding a new one in just hours. We characterized the structure and composition of the byssus biointerface using histology, confocal Raman mapping, phase contrast–enhanced microcomputed tomography, and advanced electron microscopy, revealing a sophisticated junction consisting of abiotic biopolymer sheets interdigitated between living extracellular matrix. The sheet surfaces are in intimate adhesive contact with billions of motile epithelial cilia that control biointerface strength and stem release through their collective movement, which is regulated neurochemically. We posit that this may involve a complex sensory pathway by which sessile mussels respond to environmental stresses to release and relocate.

Editor’s summary

There are many strategies in nature and biomedicine for establishing strong connections between living tissue and nonliving surfaces, but the mechanisms for separating these biointerfaces quickly and on demand are less well understood. Mytilus mussels can strongly adhere to inorganic surfaces, but they can also rapidly detach when threatened. Sivasundarampillai et al . use advanced imaging and spectroscopy methods to study the detachment process (see the Perspective by Pan and Li). They found that the responsiveness of this quick release relies on the oscillating motion of cilia and subsequently the change of mechanical interaction between the byssus stem and mussel foot tissues. The beating movement can be influenced by the application of serotonin and dopamine, thus implicating neurotransmitters in controlling the mechanical interaction between living and nonliving tissues. —Marc S. Lavine

Abstract

Mussels create a quick-release interface between living and nonliving material with neurochemically regulated strength.