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The RNA-chaperone Hfq catalyses the annealing of bacterial small RNAs (sRNAs) with target mRNAs to regulate gene expression in response to environmental stimuli. Hfq acts on a diverse set of sRNA-mRNA pairs using a variety of different molecular mechanisms. Here, we present an unusual crystal structure showing two Hfq-RNA complexes interacting via their bound RNA molecules. The structure contains two Hfq 6 :A 18  RNA assemblies positioned face-to-face, with the RNA molecules turned towards each other and connected via interdigitating base stacking interactions at the center. Biochemical data further confirm the observed interaction, and indicate that RNA-mediated contacts occur between Hfq-RNA complexes with various (ARN) X  motif containing RNA sequences  in vitro , including the stress response regulator OxyS and its target,  fhlA . A systematic computational survey also shows that phylogenetically conserved (ARN) X  motifs are present in a subset of sRNAs, some of which share similar modular architectures. We hypothesise that Hfq can co-opt RNA-RNA base stacking, an unanticipated structural trick, to promote the interaction of (ARN) X  motif containing sRNAs with target mRNAs on a “speed-dating” fashion, thereby supporting their regulatory function.

Intermolecular base stacking mediates RNA-RNA interaction in a crystal structure of the RNA chaperone Hfq