Emergent mechanics of biological structures

Abstract

Mechanical force organizes life at all scales, from molecules to cells and tissues. Although we have made remarkable progress unraveling the mechanics of life's individual building blocks, our understanding of how they give rise to the mechanics of larger-scale biological structures is still poor. Unlike the engineered macroscopic structures that we commonly build, biological structures are dynamic and self-organize: they sculpt themselves and change their own architecture, and they have structural building blocks that generate force and constantly come on and off. A description of such structures defies current traditional mechanical frameworks. It requires approaches that account for active force-generating parts and for the formation of spatial and temporal patterns utilizing a diverse array of building blocks. In this Perspective, we term this framework "emergent mechanics." Through examples at molecular, cellular, and tissue scales, we highlight challenges and opportunities in quantitatively understanding the emergent mechanics of biological structures and the need for new conceptual frameworks and experimental tools on the way ahead.

FIGURE 1:

Challenges in emergent mechanics. Biological structures are dynamic and self-organize: their building blocks come on and off on their own, whole structures transform to take new shapes and functions, and their building blocks can consume energy and generate force. Not only do these structures interweave 1) temporal, 2) architectural, and 3) active force-generation dynamics, but they do so across length scales (from nanometers to meters) and time scales (from milliseconds to days). New theoretical frameworks and experimental approaches that integrate these three aspects will provide headway in understanding the emergent mechanics of biological structures.

FIGURE 2:

Macromolecular structures and cellular ensembles show conceptual similarities in how forces flow through them, although at different length scales. (A) The spindle is one example of a macromolecular structure with changing force propagation paths (Elting, Hueschen, et al., 2014; Sikirzhytski, Magidson, et al., 2014). Dynamic restructuring of these paths under internal and external perturbations is crucial to the robustness of chromosome segregation. (B) Similarly, an ensemble of cells under internal and external forces deforms and restructures itself, rerouting forces (see line path thickness) passing through individual cells. Owing to the dynamic nature of cell–cell interactions, cellular ensembles can show surprising behaviors: they can flow like a fluid and yet sustain forces like a solid.