Abstract <p>In fluid-filled chambers, the motion of chemically active cilia tethered to soft substrates can deform the underlying layer and thus modify the delicate interplay between chemistry and mechanics in the system. To determine the effect of chemo–mechanical interactions, we developed computational models to simulate the system’s dynamics when chemical reactions at enzyme-coated cilia and substrates spontaneously generate fluid vortices. The flowing fluids, in turn, morph the ciliated layers into controllable shapes, including “scrolls,” “envelopes,” and convex “bridges,” depending on the competition between the system’s chemical reactivity and mechanical properties. Through this model, we designed a ciliated substrate that spontaneously and repeatedly rolls into a “scroll” and unrolls into a flat surface, showing a significant level of autonomous behavior. Our findings yield design rules for facilitating specific applications of fluidic devices and highlight the importance of interactions between mobile cilia and the underlying soft layer in both biological and synthetic systems.</p> Graphical abstract <p>With addition of appropriate reactants, catalyst-coated micro-posts produce fluid flows that deform both flexible elastic layer and the posts.</p> Impact statement <p>Cilia are microscale flexible filaments that are anchored to the soft tissue in, for example, the lungs, inner ears, and stomach and perform functions that are essential to our viability. Theoretical and experimental studies of biological and synthetic cilia typically do not consider the elasticity of the underlying substrate that anchors the cilia, nor the energy transduction from chemical reactions that fuels their mutual interactions. Hence, we lack detailed knowledge about the chemical and mechanical cues that enable communication between the cilia, substrate, and surrounding fluid flowing in the body. To gain further insight into forces affecting the cilial behavior, we developed a model that encompasses the elasticity of the substrate, the flexibility of the cilia, and the enzymatic reactions that contribute to the fluid motion. Our results reveal how chemically driven fluid motion affects the shape of both the bendable cilia and deformable soft substrate, and in turn how the deformed surfaces alter the flow behavior and thus trigger continuous feedback among chemistry, the fluid and the surfaces. Understanding the latter feedback is critical to unraveling the cilia’s biological behavior and fabricating synthetic analogues that expand the functionality of fluidic devices.</p>