Every living cell is a compartmentalized out-ofequilibrium system exquisitely able to convert chemical energy into function. In order to maintain homeostasis, the flux of metabolites is tightly controlled by regulatory enzymatic networks. A crucial prerequisite for the development of lifelike materials is the construction of synthetic systems with compartmentalized reaction networks that maintain out-of-equilibrium function. Here, we aim for autonomous movement as an example of the conversion of feedstock molecules into function. The flux of the conversion is regulated by a rationally designed enzymatic reaction network with multiple feedforward loops. By compartmentalizing the network into bowl-shaped nanocapsules the output of the network is harvested as kinetic energy. The entire system shows sustained and tunable microscopic motion resulting from the conversion of multiple external substrates. The successful compartmentalization of an out-of-equilibrium reaction network is a major first step in harnessing the design principles of life for construction of adaptive and internally regulated lifelike systems.