A cyanobacterium,Synechocystissp. PCC 6803, contains a lipid with triacylglycerol-like TLC mobility but its identity and physiological roles remain unknown. Here, on ESI-positive LC-MS2analysis, it is shown that the triacylglycerol-like lipid (lipid X) is related to plastoquinone and can be grouped into two subclasses, Xaand Xb, the latter of which is esterified by 16:0 and 18:0. This study further shows that aSynechocystishomolog of type-2 diacylglycerol acyltransferase genes,slr2103, is essential for lipid X synthesis: lipid X disappears in aSynechocystis slr2103-disruptant whereas it appears in anslr2103-overexpressing transformant (OE) ofSynechococcus elongatusPCC 7942 that intrinsically lacks lipid X. Theslr2103disruption causesSynechocystiscells to accumulate plastoquinone-C at an abnormally high level whereasslr2103overexpression inSynechococcuscauses the cells to almost completely lose it. It is thus deduced thatslr2103encodes a novel acyltransferase that esterifies 16:0 or 18:0 with plastoquinone-C for the synthesis of lipid Xb. Characterization of theslr2103-disruptant inSynechocystisshows thatslr2103contributes to sedimented-cell growth in a static culture, and to bloom-like structure formation and its expansion by promoting cell aggregation and floatation upon imposition of saline stress (0.3-0.6 M NaCl). These observations provide a basis for elucidation of the molecular mechanism of a novel cyanobacterial strategy to acclimatize to saline stress, and one for development of a system of seawater-utilization and economical harvesting of cyanobacterial cells with high-value added compounds, or blooming control of toxic cyanobacteria.