Sliding-before-breaking governs deformation in chitinous extracellular matrices reinforced by strong, fatigue-resistant chitin
8 affiliations
- 1Bioproducts Institute, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
- 2Department of Chemical and Biological Engineering, The University of British Columbia, Vancouver, BC V6T 1Z3, Canada
- 3Department of Biology, Hong Kong Baptist University, Hong Kong SAR 999077, China
- 4University of Tennessee/Oak Ridge National Laboratory Center for Molecular Biophysics, Oak Ridge National Laboratory, Oak Ridge, TN 37831
- 5Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831
- 6Department of Colloid Chemistry, Max Planck Institute of Colloids and Interfaces, Am Mühlenberg 1, Potsdam 14476, Germany
- 7Department of Wood Science, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
- 8Department of Chemistry, The University of British Columbia, Vancouver, BC V6T 1Z1, Canada
Abstract
Many fibrous biological materials combine high strength with the ability to undergo permanent shape change, a balance that remains difficult to replicate synthetically. In twisted, plywood-like architectures, the origin of irreversible deformation remains unresolved: does strain arise from covalent bond scission or from coordinated interfacial processes across hierarchical scales? Here, we use the chitin-based protective tubes of vestimentiferan deep-sea tubeworms (Siboglinidae: Vestimentifera) as a model system to address this question. By integrating multiscale simulations with experimental measurements, we show that the chitin covalent backbone resists tensile rupture and exhibits negligible fatigue under physiologically relevant loading. Instead, mechanical stress is dissipated through controlled sliding within and between chitin nanostructures as well as across chitin–protein interfaces, leading to cumulative, irreversible deformation across length scales. Covalent bond rupture of chitin, the primary load-bearing component of the tube, becomes energetically accessible only when mechanical loading acts in concert with enzyme-mediated bond cleavage. These findings establish a sliding-before-breaking principle, in which backbone stability preserves structural integrity while regulated interfacial sliding governs energy dissipation and growth. This principle provides a general framework for the design of hierarchical materials that combine fatigue resistance with adaptive deformation.
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BibTeX
@article{wan2026slidingbeforebreaking,
title = {{Sliding-before-breaking governs deformation in chitinous extracellular matrices reinforced by strong, fatigue-resistant chitin}},
author = {Zhangmin Wan and Chris Zhou and Maëva Perez and Jian-Wen Qiu and Zihui Shen and Xin Lu and Jie Wu and Shuyuan Cui and Yan Yu and Xun Niu and Ran Bi and Jeremy C. Smith and Simcha Srebnik and Orlando J. Rojas},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
year = {2026},
month = sep,
doi = {10.1073/pnas.2613826123},
url = {https://doi.org/10.1073/pnas.2613826123},
note = {CC BY-NC-ND 4.0},
}
RIS
TY - JOUR
TI - Sliding-before-breaking governs deformation in chitinous extracellular matrices reinforced by strong, fatigue-resistant chitin
AU - Zhangmin Wan
AU - Chris Zhou
AU - Maëva Perez
AU - Jian-Wen Qiu
AU - Zihui Shen
AU - Xin Lu
AU - Jie Wu
AU - Shuyuan Cui
AU - Yan Yu
AU - Xun Niu
AU - Ran Bi
AU - Jeremy C. Smith
AU - Simcha Srebnik
AU - Orlando J. Rojas
PY - 2026
DA - 2026/09/23
JO - Proceedings of the National Academy of Sciences of the United States of America
DO - 10.1073/pnas.2613826123
UR - https://doi.org/10.1073/pnas.2613826123
AB - Many fibrous biological materials combine high strength with the ability to undergo permanent shape change, a balance that remains difficult to replicate synthetically. In twisted, plywood-like architectures, the origin of irreversible deformation remains unresolved: does strain arise from covalent bond scission or from coordinated interfacial processes across hierarchical scales? Here, we use the chitin-based protective tubes of vestimentiferan deep-sea tubeworms (Siboglinidae: Vestimentifera) as a model system to address this question. By integrating multiscale simulations with experimental measurements, we show that the chitin covalent backbone resists tensile rupture and exhibits negligible fatigue under physiologically relevant loading. Instead, mechanical stress is dissipated through controlled sliding within and between chitin nanostructures as well as across chitin–protein interfaces, leading to cumulative, irreversible deformation across length scales. Covalent bond rupture of chitin, the primary load-bearing component of the tube, becomes energetically accessible only when mechanical loading acts in concert with enzyme-mediated bond cleavage. These findings establish a sliding-before-breaking principle, in which backbone stability preserves structural integrity while regulated interfacial sliding governs energy dissipation and growth. This principle provides a general framework for the design of hierarchical materials that combine fatigue resistance with adaptive deformation.
SN - 0027-8424
SN - 1091-6490
ER -