Hidden length lets collagen buffer mechanical and chemical stress.

Collagen, the most abundant protein in the human body, must withstand high mechanical loads due to its structural role in tendons, skin, bones, and other connective tissue. It was recently found that tensed collagen creates mechanoradicals by homolytic bond scission. We here employ scale-bridging simulations to determine the influence of collagen's mesoscale fibril structure on molecular breakages, combining atomistic molecular dynamics simulations with a newly developed mesoscopic ultra-coarse-grained description of a collagen fibril. Our simulations identify a conserved structural feature, a length difference of the two helices between pairs of crosslinks, to play a critical role. The release of the extra hidden length enables collagen to buffer mechanical stress. At the same time, this topology funnels ruptures such that the potentially harmful mechanoradicals are readily stabilized, buffering the arising oxidative stress. Our results suggest collagen's hidden length to exploit a sweet spot in the trade-off between breakage specificity and strength.