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Many cyanobacteria, which use light as an energy source via photosynthesis, have evolved the ability to guide their movement toward or away from a light source. This process, termed “phototaxis,” enables organisms to localize in optimal light environments for improved growth and fitness. Mechanisms of phototaxis have been studied in the coccoid cyanobacteriumSynechocystissp. strain PCC 6803, but the rod-shapedSynechococcus elongatusPCC 7942, studied for circadian rhythms and metabolic engineering, has no phototactic motility. In this study we report a recent environmental isolate ofS. elongatus, the strain UTEX 3055, whose genome is 98.5% identical to that of PCC 7942 but which is motile and phototactic. A six-gene operon encoding chemotaxis-like proteins was confirmed to be involved in phototaxis. Environmental light signals are perceived by a cyanobacteriochrome, PixJ_Se(Synpcc7942_0858), which carries five GAF domains that are responsive to blue/green light and resemble those of PixJ fromSynechocystis. Plate-based phototaxis assays indicate that UTEX 3055 uses PixJ_Seto sense blue and green light. Mutation of conserved functional cysteine residues in different GAF domains indicates that PixJ_Secontrols both positive and negative phototaxis, in contrast to the multiple proteins that are employed for implementing bidirectional phototaxis inSynechocystis.