Viscoelastic analysis of mussel threads reveals energy dissipative mechanisms

Marcela Areyano*, Eric Valois, Ismael Sanchez Carvajal, Ivan Rajkovic, William R. Wonderly, Attila Kossa, Robert M. McMeeking, J. Herbert Waite

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)

Abstract

Mussels use byssal threads to secure themselves to rocks and as shock absorbers during cyclic loading from wave motion. Byssal threads combine high strength and toughness with extensibility of nearly 200%. Researchers attribute tensile properties of byssal threads to their elaborate multi-domain collagenous protein cores. Because the elastic properties have been previously scrutinized, we instead examined byssal thread viscoelastic behaviour, which is essential for withstanding cyclic loading. By targeting protein domains in the collagenous core via chemical treatments, stress relaxation experiments provided insights on domain contributions and were coupled with in situ small-angle X-ray scattering to investigate relaxation-specific molecular reorganizations. Results show that when silk-like domains in the core were disrupted, the stress relaxation of the threads decreased by nearly 50% and lateral molecular spacing also decreased, suggesting that these domains are essential for energy dissipation and assume a compressed molecular rearrangement when disrupted. A generalized Maxwell model was developed to describe the stress relaxation response. The model predicts that maximal damping (energy dissipation) occurs at around 0.1 Hz which closely resembles the wave frequency along the California coast and implies that these materials may be well adapted to the cyclic loading of the ambient conditions.

Original languageEnglish
Article number20210828
Number of pages10
JournalJournal of the Royal Society Interface
Volume19
Issue number188
Early online date23 Mar 2022
DOIs
Publication statusPublished - Mar 2022

Bibliographical note

Funding
This work was supported by the Materials Research Science and Engineering Center (MRSEC) Program of the National Science Foundation (NSF) under award no. DMR 1720256 (IRG-3). A.K. and this research was supported by the Hungarian National Research, Development and Innovation Office (NKFI FK 128662). Additionally, I.S.C. and this research was supported by the LSAMP programme of the National Science Foundation under award no. HRD-1826900. M.A. acknowledges support of the NSF California LSAMP Bridge to the Doctorate Fellowship under grant no. HRD-1701365. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under contract no. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (P30GM133894). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH.

Acknowledgements
The authors acknowledge the use of the Microfluidics Laboratory within the California NanoSystems Institute, supported by the University of California, Santa Barbara and the University of California, Office of the President. The authors thank Ram Seshadri for providing feedback on the manuscript. The authors also thank Dariya Ignatenko for assisting in making buffer solutions.

Data Availability Statement

Data and code generated through this work are made available at FigShare (doi:10.6084/m9.figshare.17563055).

The data are provided in electronic supplementary material [60].

Keywords

  • biomaterials
  • collagenous hierarchical material
  • generalized Maxwell model
  • stress relaxation
  • viscoelasticity
  • Silk
  • Animals
  • Software
  • Bivalvia/chemistry

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