Prochlorococcus is a marine picocyanobacterium with a streamlined genome that is adapted to different ecological niches in the oligotrophic oceans. There are currently >20 regulatory small RNAs (sRNAs) that have been identified in the model strain Prochlorococcus MED4. While most of these sRNAs are ecotype-specific, sRNA homologs of Yfr1 and of the Yfr2 family are widely found throughout the cyanobacterial phylum. Although they were identified 13 yrs ago, the functions of Yfr1 and Yfr2 have remained unknown. We observed a strong induction of two Yfr2 sRNA homologs of Prochlorococcus MED4 during high light stress and nitrogen starvation. Several Prochlorococcus and marine Synechococcus yfr2 promoter regions contain a conserved motif we named CGRE1 (cyanobacterial GntR family transcriptional regulator responsive element 1). Using the conserved promoter region as bait in a DNA affinity pull-down assay we identified the GntR family transcriptional regulator PMM1637 as a binding partner. Similar to Yfr2, homologs of PMM1637 are universally and exclusively found in cyanobacteria. We suggest that PMM1637 governs the induction of gene expression of Yfr2 homologs containing CGRE1 in their promoters under nitrogen-depleted and high-light stress conditions.