The fibrillar-level mechanisms of mutability in echinoderm connective tissue analysed using in situ synchrotron small-angle X-ray scatteringPart of:
The collagenous matrix is a critical biomechanical component of soft structural biological tissues (skin, bone, heart valves) in both vertebrates and invertebrates . However, in contrast to tissues like muscle, most collagenous tissues serve largely passive mechanical roles. A striking exception is the mutable collagenous tissue (MCT) of echinoderms (like sea cucumbers or starfish), which can change its mechanical state from flaccid to stiff within seconds in response to external stimuli such as touch or predatory attack . However, the nanoscale mechanisms enabling mutability have not been investigated experimentally. Here, we used in situ synchrotron small-angle X-ray diffraction (SAXD) to map temporal changes in collagen fibrillar ultrastructure in different mechanical states of MCT from sea cucumber dermis . On application of tensile strain, we find a higher proportion of strain taken up by the fibrils when the tissue is macroscopically stiffened, compared to when it is in the soft state. A staggered model of anisotropic collagen fibrils surrounded by an extrafibrillar matrix of proteoglycans, water and neuroeffector molecules is used to interpret the data. Our results show that mutability alterations in tissue mechanics - concurrent with small-scale fibrillar behaviour – can be explained only if the interfibrillar matrix changes its mechanical state while the collagen fibrils remain mechanically unchanged. Our findings may have applications in design of bioinspired stimuli-responsive hydrogels, linking echinoderm biomechanics to molecular alterations and in testing the efficacy of synthetic peptides for softening or stiffening collagenous tissue.