Sponges are the oldest basal metazoans and host a dense and diverse microbial population that can include symbiotic cyanobacteria. The latter provide an additional source of organic carbon, and thus may play a pivotal role within the holobiont. Numerous studies have described the genetic diversity of sponge-cyanobacteria symbioses, but little is known of the potential interactions of cyanobacteria and the heterotrophic microbial community found inside the same sponge, or the genetic adaptations of cyanobacteria to `life in symbiosis` with a sponge host. We used a facultative sponge-cyanobacteria model system (Petrosia ficiformis-Synechococcus feldmanni) to test the effect of cyanobacterial presence on the diversity of the heterotrophic microbial consortium. The study provided evidence that biogeography rather than presence of photosymbionts is the main factor influencing the heterotrophic microbial community in the sponge P. ficiformis. Moreover, we studied the genomic attributes of obligatory cyanobacterial symbionts compared to free-living cyanobacteria to shed light on genomic adaptations and on intra-species genomic divergence in the symbiotic Synechococcus spongiarum. From the analysis of the draft genomes of four obligatory cyanobacterial symbionts we were able to reveal unique common features of these symbionts. These included a higher proportion of genes involved in modification and recombination that may relate to horizontal gene transfer, genes likely involved in host-microbe recognition mechanisms (including eukaryotic like proteins) and phage-resistance mechanisms. Genome reduction in the symbionts was characterized by lower proportion of genes involved in signal transduction mechanisms and cell wall/membrane biogenesis possibly reflecting a more stable environment inside the host.