The mechanical properties of cells and tissues play a well-known role in physiology and disease. The model organism Caenorhabditis elegans exhibits mechanical properties that are still poorly understood, but are thought to be dominated by its collagen-rich outer cuticle. We use a microfluidic technique to reveal that the worm responds linearly to low applied hydrostatic stress, exhibiting a volumetric compression with a bulk modulus, κ = 140 ± 20 kPa; applying negative pressures leads to volumetric expansion of the worm, with a similar bulk modulus. Surprisingly, however, we find that a variety of collagen mutants and pharmacological perturbations targeting the cuticle do not impact the bulk modulus. Moreover, the worm exhibits dramatic stiffening at higher stresses—behavior that is also independent of the cuticle. The stress-strain curves for all conditions can be scaled onto a master equation, suggesting that C. elegans exhibits a universal elastic response dominated by the mechanics of pressurized internal organs.

Introduction

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Hebrank J.H. Shark skin: function in locomotion. Beneath the cuticle sits the pseudocoelom, an internal cavity that surrounds the worm’s digestive tract and supports its organs. Local measurements of the internal pressure in the pseudocoelom of Ascaris, a large, parasitic relative of C. elegans, have been performed using a microscale manometer inserted directly into the body cavity. These measurements suggest an internal pressure in the range of 50–100 kPa (). Internal pressure is thought to induce prestrain in taut, helical collagen fiber bundles, causing a decrease in strain energy under bending that induces the curved appearance of many adult nematodes (). Experiments on these collagen fibers in larger organisms such as fish and sharks suggest that they become stiffer under extension, and may couple to interfiber matrices throughout the organism’s body in order to increase the range of body shapes that are elastically stable ().

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Dalnoki-Veress K. Viscoelastic properties of the nematode Caenorhabditis elegans, a self-similar, shear-thinning worm. Despite the high stiffness measurements reported for the worm cuticle, an analysis based on the bending moments observed in the worm’s undulatory swimming gait leads to a significantly lower estimate for the Young’s modulus for the entire worm, 3.77 kPa (); the mechanical loading in this experiment was provided by the worm’s own muscles as it swims, complicating interpretation and possibly underlying the low modulus value. Another recent study measured the worm’s bending modulus using deflection of the entire body under actuation from a single point (). Calculating the Young’s modulus of the worm’s body yields a value ranging from 110 kPa to 1.3 MPa, depending on whether the worm is modeled as a uniform cylinder or cylindrical shell (). The large range of reported values highlights our poor understanding of the mechanical properties of C. elegans. There is a clear need for elucidating the role of the cuticle, as well as the interplay of internal and external pressure, in the mechanics of the whole worm.