Hygroscopic biological matter in plants, fungi and bacteria make up a large fraction of Earth’s biomass 1. Although metabolically inert, these water-responsive materials exchange water with the environment and actuate movement 2–5 and have inspired technological uses 6,7. Despite the variety in chemical composition, hygroscopic biological materials across multiple kingdoms of life exhibit similar mechanical behaviours including changes in size and stiffness with relative humidity 8–13. Here we report atomic force microscopy measurements on the hygroscopic spores 14,15 of a common soil bacterium and develop a theory that captures the observed equilibrium, non-equilibrium and water-responsive mechanical behaviours, finding that these are controlled by the hydration force 16–18. Our theory based on the hydration force explains an extreme slowdown of water transport and successfully predicts a strong nonlinear elasticity and a transition in mechanical properties that differs from glassy and poroelastic behaviours. These results indicate that water not only endows biological matter with fluidity but also can—through the hydration force—control macroscopic properties and give rise to a ‘hydration solid’ with unusual properties. A large fraction of biological matter could belong to this distinct class of solid matter.
Bibliographical noteWe acknowledge A. Driks (Department of Microbiology and Immunology, Loyola University Chicago, Maywood, IL, USA) who passed away before the completion of the work for contributing spores, and for discussions that informed the hygroelastic theory and for suggesting the use of known sieving properties of spores as an estimate of pore size. Funding was provided by US Department of Energy (DOE) Early Career Research Program, Office of Science, Basic Energy Sciences (BES), under award no. DE-SC0007999 (Fig. and experimental data in Figs. and); by the Office of Naval Research, under award nos. N00014-19-1-2200 (Fig. and theoretical analyses in Figs. and) and N00014-21-1-4004 (theoretical analyses in Figs. and); by the National Institute of General Medical Sciences of the National Institutes of Health, under award nos. R35GM141953 (to J.D.) and R35GM145382 (to O.S.); and by the David and Lucile Packard Fellows Program. We acknowledge the use of facilities and instrumentation supported by NSF through the Columbia University, Columbia Nano Initiative, and the Materials Research Science and Engineering Center DMR-2011738.
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.