Inside cells, complex metabolic reactions are distributed
across the modular compartments of organelles1,2.
Reactions in organelles have been recapitulated in vitro by
reconstituting functional protein machineries into membrane
systems3–5. However, maintaining and controlling these
reactions is challenging. Here we designed, built, and
tested a switchable, light-harvesting organelle that provides
both a sustainable energy source and a means of directing
intravesicular reactions. An ATP (ATP) synthase and two
photoconverters (plant-derived photosystem II and bacteriaderived proteorhodopsin) enable ATP synthesis. Independent
optical activation of the two photoconverters allows dynamic
control of ATP synthesis: red light facilitates and green light
impedes ATP synthesis. We encapsulated the photosynthetic
organelles in a giant vesicle to form a protocellular system
and demonstrated optical control of two ATP-dependent
reactions, carbon fixation and actin polymerization, with
the latter altering outer vesicle morphology. Switchable
photosynthetic organelles may enable the development of
biomimetic vesicle systems with regulatory networks that
exhibit homeostasis and complex cellular behaviors.