The GacS/A-RsmA Signal Transduction Pathway Controls the Synthesis of Alkylresorcinol Lipids that Replace Membrane Phospholipids during Encystment of Azotobacter vinelandii SW136.

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Azotobacter vinelandii is a soil bacterium that undergoes a differentiation process that forms cysts resistant to desiccation. During encystment, a family of alkylresorcinols lipids (ARs) are synthesized and become part of the membrane and are also components of the outer layer covering the cyst, where they play a structural role. The synthesis of ARs in A. vinelandii has been shown to occur by the activity of enzymes encoded in the arsABCD operon. The expression of this operon is activated by ArpR, a LysR-type transcriptional regulator whose transcription occurs during encystment and is dependent on the alternative sigma factor RpoS. In this study, we show that the two component response regulator GacA, the small RNA RsmZ1 and the translational repressor protein RsmA, implicated in the control of the synthesis of other cysts components (i.e., alginate and poly-ß-hydroxybutyrate), are also controlling alkylresorcinol synthesis. This control affects the expression of arsABCD and is exerted through the regulation of arpR expression. We show that RsmA negatively regulates arpR expression by binding its mRNA, repressing its translation. GacA in turn, positively regulates arpR expression through the activation of transcription of RsmZ1, that binds RsmA, counteracting its repressor activity. This regulatory cascade is independent of RpoS. We also show evidence suggesting that GacA exerts an additional regulation on arsABCD expression through an ArpR independent route.