The prochlorophytes are a diverse group of photosynthetic prokaryotes that fall within the cyanobacterial lineage, yet lack phycobilisomes as light harvesting structures. Instead, the prochlorophytes have a light-harvesting apparatus composed of the higher plant pigments chlorophylls a and b. This review discusses the evolutionary relationships among these bacteria, with focus on the structure and function of the photosynthetic apparatus. This analysis yields a consensus from studies both on Prochloron sp. and Prochlorothrix hollandica as to how the thylakoid membrane is organized. Overall, we propose that the structure of the light-harvesting complexes (LHC) from prochlorophytes is very different from those of chloroplast systems, and is evolutionarily very ancient. The functional association of the light-harvesting apparatus with photosystem I (PSI) in both Prochlorothrix and Prochloron, as well as a demonstrated capacity for PSI-dependent anoxygenic photosynthesis in Prochlorothrix, may indicate that there is an increased dependence on cyclic photophosphorylation in these organisms. Finally, the structure of the prochlorophyte thylakoid membrane is discussed with respect to the forces that drive thylakoid membrane stacking in prochlorophytes and chloroplasts. We suggest that the light-harvesting structures in prochlorophytes play little, if any, role in this process.