SliP4 is a 37 amino acids small protein that is strongly induced when the cyanobacterium Synechocystis is exposed to high-light conditions. Deletion mutants exhibit a light-sensitive phenotype due to impaired cyclic electron flow and state transitions. Here, we investigated the consequences of SliP4 deficiency on the high-light acclimation. The ∆sliP4 mutant exhibited a fully intact gene regulatory response 30 min after shifting the light intensity from 50 to 250 μmol photons m-2 s-1 mediated by the RpaB-PsrR1 system. However, 48 h after the shift to high light, the mutant increased the production of extracellular polysaccharides and the cells started to aggregate, effectively reducing the potential impact of light stress effects caused by the impaired capacity for cyclic electron flow and state transitions. This effect included the upregulation of xssA-E and xssN-P genes for the production of synechan, a sulfated exopolysaccharide. Our results show that the unicellular cyanobacterium Synechocystis can compensate the crucial role of SliP4 by the activation of a population-level response to cope with light stress conditions and reveal several genes involved in this response.