The self-driven organization of model protocells into higher-order nested cytomimetic systems with coordinated structural and functional relationships offers a step toward the autonomic implementation of artificial multicellularity. Here, we describe an endosymbiotic-like pathway in which proteinosomes are captured within membranized alginate/silk fibroin coacervate vesicles by guest-mediated reconfiguration of the host protocells. We demonstrate that interchange of coacervate vesicle and droplet morphologies through proteinosome-mediated urease/glucose oxidase activity produces discrete nested communities capable of integrated catalytic activity and selective disintegration. The self-driving capacity is modulated by an internalized fuel-driven process using starch hydrolases sequestered within the host coacervate phase, and structural stabilization of the integrated protocell populations can be achieved by on-site enzyme-mediated matrix reinforcement involving dipeptide supramolecular assembly or tyramine-alginate covalent cross-linking. Our work highlights a semi-autonomous mechanism for constructing symbiotic cell-like nested communities and provides opportunities for the development of reconfigurable cytomimetic materials with structural, functional, and organizational complexity.