Several strains of unicellular cyanobacteria from the culture collection of St. Petersburg State University, St. Petersburg, Russia (CALU), which were preliminary identified as Synechocystis sp., are reclassified in the new genus Altericista. Three new species are proposed, A. lacusladogae, A. violacea, and A. variichlora. The last species produces accessory chlorophylls d and f in cultures illuminated by far-red light, an attribute rarely observed in cyanobacteria, especially in unicellular strains. This genus is morphologically similar to Synechocysis having coccoid cells that divide in two successive planes at right angles, containing no sheath or capsule, and having the lamellar system represented by peripheral concentric thylakoids. Altericista shows ecological, biochemical, and physiological characters unlike those in Synechocystis and has the distinguishing phenotypic characters as follows: freshwater, non-halotolerant ecotype; palmitate and α-linoleate as major fatty acids; and the ability to photoacclimate, including several types of complementary chromatic adaptation. Genetic differences from Synechocystis sp. include 16S rRNA, rpoC1, and rbcL gene sequences, as well as sequence and folding of 16S-23S ITS.