The extraordinary joint material of an articulated coralline alga. II. Modeling the structural basis of its mechanical properties

Abstract

By incorporating joints into their otherwise rigid fronds, erect coralline algae have evolved to be as flexible as other seaweeds, which allows them to thrive -and even dominate space -on wave-washed shores around the globe. However, to provide the required flexibility, the joint tissue of Calliarthron cheilosporioides, a representative articulated coralline alga, relies on an extraordinary tissue that is stronger, more extensible and more fatigue resistant than that of other algae. Here, we used the results from recent experiments to parameterize a conceptual model that links the microscale architecture of cell walls to the adaptive mechanical properties of joint tissue. Our analysis suggests that the theory of discontinuous fiber-wound composite materials (with cellulose fibrils as the fibers and galactan gel as the matrix) can explain key aspects of the material's mechanics. In particular, its adaptive viscoelastic behavior can be characterized by two, widely separated time constants. We speculate that the short time constant (∼14 s) results from the viscous response of the matrix to the change in cell-wall shape as a joint is stretched, a response that allows the material both to remain flexible and to dissipate energy as a frond is lashed by waves. We propose that the long time constant (∼35 h), is governed by the shearing of the matrix between cellulose fibrils. The resulting high apparent viscosity ensures that joints avoid accumulating lethal deformation in the course of a frond's lifetime. Our synthesis of experimental measurements allows us to draw a chain of mechanistic inference from molecules to cell walls to fronds and community ecology.

The extraordinary joint material of an articulated coralline alga. I. Mechanical characterization of a key adaptation

“…In addition, the results described here in the context of genicular function can also be used in combination with previous findings to understand how the material properties of C. cheilosporioides' genicula can be explained by the microscale structure of genicular cell walls. We address this task in the companion paper (Denny and King, 2016).…”

“…This and our companion paper (Denny and King, 2016) are a first effort at such a synthesis. To gain a mechanistic understanding of C. cheilosporioides' genicular material, we used experimental data to fill in the missing pieces of information, and, in the companion paper, we propose a simple conceptual model that provides a mechanistic explanation for the behavior of this exceptional material.…”

“…To what extent can we use a detailed description of genicular material properties to build an understanding of C. cheilosporioides' whole-frond mechanics, and thereby its success in an ecological context? We address questions 1 and 2 in this report; we address question 3 in the companion paper (Denny and King, 2016).…”

Marine-Derived Polymeric Materials and Biomimetics: An Overview

“…As they provide mechanical support for the structure of microalgae, it is possible to use them for materials that retain the key features: matrix mechanics and permeability; the ability to sequester and to deliver drugs, proteins, and or nucleic acids; provide receptor-or enzyme-mediated cell-matrix interactions [94]. Existing examples include the incorporation of specific nanofibrils of cellulose in polysaccharides matrices provides adaptive viscoelastic behaviour and results in tissue that is stronger, more extensible and more fatigue resistant [95,96]. Calcareous coralline algae were recently shown to produce chitin and collagen-like proteins, with the two biopolymers likely playing a role in the biomineralization process of the algal skeletons [93,97].…”

Transcriptome of the coralline alga Calliarthron tuberculosum (Corallinales, Rhodophyta) reveals convergent evolution of a partial lignin biosynthesis pathway

“…Among the principal chemical components of wood, lignins in plant secondary cell walls help reinforce tissue mechanical properties, permit hydraulic transport, and increase pathogen resistance [27, 28]. In the articulated coralline C. cheilosporioides , lignins were found predominantly within decalcified flexible joints, called genicula [23], that have remarkable biomechanical properties, permitting this articulated coralline species to thrive along wave-battered coastlines [29, 30].…”