Materials science and mechanosensitivity of living matter

Abstract

Living systems are composed of molecules that are synthesized by cells that use energy sources within their surroundings to create fascinating materials that have mechanical properties optimized for their biological function. Their functionality is a ubiquitous aspect of our lives. We use wood to construct furniture, bacterial colonies to modify the texture of dairy products and other foods, intestines as violin strings, bladders in bagpipes, and so on. The mechanical properties of these biological materials differ from those of other simpler synthetic elastomers, glasses, and crystals. Reproducing their mechanical properties synthetically or from first principles is still often unattainable. The challenge is that biomaterials often exist far from equilibrium, either in a kinetically arrested state or in an energy consuming active state that is not yet possible to reproduce de novo. Also, the design principles that form biological materials often result in nonlinear responses of stress to strain, or force to displacement, and theoretical models to explain these nonlinear effects are in relatively early stages of development compared to the predictive models for rubberlike elastomers or metals. In this Review, we summarize some of the most common and striking mechanical features of biological materials and make comparisons among animal, plant, fungal, and bacterial systems. We also summarize some of the mechanisms by which living systems develop forces that shape biological matter and examine newly discovered mechanisms by which cells sense and respond to the forces they generate themselves, which are resisted by their environment, or that are exerted upon them by their environment. Within this framework, we discuss examples of how physical methods are being applied to cell biology and bioengineering.

To seal a wound, caterpillars transform blood from a viscous to a viscoelastic fluid in a few seconds

“…This analysis emphasizes the importance of interfacial forces in gathering and holding hemocytes together during the development of primary clots. In recent years, the fruitful analogy between the cell aggregates of developing tissues and liquids with a viscoelastic rheology has offered new perspectives in biological soft matter (Steinberg, 2007;Janmey et al, 2009;Gonzalez-Rodriguez et al, 2012;Foty and Steinberg, 2013;Beaune et al, 2014;Beris et al, 2021;Patteson et al, 2022). Although the mainstream research in this direction is focused on vertebrate and human blood, little is known about the material properties of insect blood.…”

A Torsion-Based Rheometer for Measuring Viscoelastic Material Properties

“…In recent years, the field of mechanobiology has emerged to study the effects of mechanical forces on biological systems (19)(20)(21). It is increasingly recognized, for example, that the mechanical properties of a cell's environment can affect many cellular functions, including motility, differentiation, and proliferation (22)(23)(24).…”

Bacteria Colonies Modify Their Shear and Compressive Mechanical Properties in Response to Different Growth Substrates

“…Living cells use physical and chemical signals from their environment to adapt their shape, size, and activity . The mechanical properties of cells and tissues are often critical to their biological function, as living materials must be rigid enough to maintain their structure yet compliant enough to change shape as needed.…”

“…Living cells use physical and chemical signals from their environment to adapt their shape, size, and activity. 1 The mechanical properties of cells and tissues are often critical to their biological function, as living materials must be rigid enough to maintain their structure yet compliant enough to change shape as needed. It is now well-known that many (though not all) animal cell types tune their shape and stiffness in response to changes in the mechanical properties of their local tissue microenvironment.…”