Cyanobacteria, as the most simple organisms to perform oxygenic photosynthesis differ from higher plants especially with respect to the thylakoid membrane structure and the antenna system used to capture light energy. Cyanobacterial antenna systems, the phycobilisomes (PBS), have been shown to be associated with Photosystem 2 (PS 2) at the cytoplasmic side, forming a PS 2-PBS-supercomplex, the structure of which is not well understood. Based on structural data of PBS and PS 2, a model for such a supercomplex is presented. Its key features are the PS 2 dimer as prerequisite for formation of the supercomplex and the antiparallel orientation of PBS-cores and the two PS 2 monomers which form the 'contact area' within the supercomplex. Possible consequences for the formation of 'superstructures' (PS 2-PBS rows) within the thylakoid membrane under so-called 'state 1' conditions are discussed. As there are also indications for specific functional connections of PBS with Photosystem 1 (PS 1) under so-called 'state 2' conditions, we show a model which reconciles the need for a structural interaction between PBS and PS 1 with the difference in structural symmetry (2-fold rotational symmetry of PBS-cores, 3-fold rotational symmetry of trimeric PS 1). Finally, the process of dynamic coupling and uncoupling of PBS to PS 1 and PS 2, based on the presented models, shows analogies to mechanisms for the regulation of photosynthetic electron flow in higher plants-despite the very different organization of their thylakoid membranes in comparison to cyanobacteria.