Microbial consortia composed of autotrophic and heterotrophic species abound in nature, yet examples of synthetic communities with mixed metabolism are limited in the laboratory. Herein, we construct artificial synthetic consortia consisting of sucrose-secreting cyanobacteria, Synechococcus elongatus PCC 7942, paired with three disparate heterotrophs: Bacillus subtilis, Escherichia coli, or Saccharomyces cerevisiae. Comparison of these different dyads highlights underlying interactions in co-culture. We witness both engineered and emergent interactions between cyanobacterium and heterotroph shared across heterotrophic species. Heterotrophs can consume carbon fixed photosynthetically by cyanobacteria while non-sucrose byproducts of photosynthesis can negatively impact heterotroph growth. Surprisingly, all tested heterotrophic species can positively impact cyanobacterial growth in co-culture in comparison to monoculture. Growth of co-cultures is witnessed in batch and continuous culture as well as on agar plates. Co-cultures persist long-term and can survive perturbation, particularly when heterotrophic sucrose uptake is enhanced and/or heterotrophic sensitivity to byproducts of photosynthetic metabolism is mitigated. This level of robustness is infrequently witnessed in synthetic microbial communities. Furthermore, by exchanging partner heterotrophs, we demonstrate flexible, phototrophic production of alpha-amylase and polyhydroxybutyrate in co-cultures containing specialized strains of B. subtilis and E. coli, respectively. Production can be improved via engineered intervention, i.e. increased efficiency growing on sucrose, showing promise for future tuning of these communities as production platforms. Altogether these synthetic microbial consortia provide a platform to study autotroph-heterotroph interactions, while demonstrating promising flexibility and stability for potential photoproduction strategies that capitalize on multi-species interactions.