| Summary: | Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus <i>Leptothoe</i> (Synechococcales). We obtained draft genomes from <i>Le. kymatousa</i> TAU-MAC 1615 and <i>Le. spongobia</i> TAU-MAC 1115, isolated from marine sponges. We identified five additional <i>Leptothoe</i> genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. <i>Le. kymatousa</i> and <i>Le. spongobia</i> have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated <i>Leptothoe</i> genomes. The sponge-associated <i>Leptothoe</i> stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of <i>Leptothoe</i> with chemically rich cyanobacteria revealed that <i>Leptothoe</i> is another promising marine cyanobacterium for the biosynthesis of novel natural products.
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