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Cells convert light or chemical energy of nutrients into other forms of energy, such as ion gradients or adenosine triphosphate (ATP). However, engineering sustained fueling pathways in synthetic systems is challenging. Inspired by endosymbionts that rely on the host cell for their nutrients, we introduce the concept of cross-feeding between synthetic submicron-size vesicles that can exchange ATP and ADP across their membranes. One population of vesicles produces and exports ATP, while a second population of vesicles takes up ATP to fuel energy-consuming reactions. The produced ADP feeds back to the first vesicles. The vesicles are a platform technology to fuel ATP-dependent processes in a sustained fashion, with potential applications in synthetic cells and nanoreactors. 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