Characterization of an Ethylene Receptor in <i>Synechocystis</i> sp. PCC 6803

In plants, ethylene functions as a hormone regulating many growth and developmental processes. Ethylene receptors in plants resemble bacterial two-component signaling systems. Because of this it, ethylene receptors are thought to have been acquired by gene transfer from the cyanobacterial endosymbiont that lead to the development of the chloroplast. However, prior to this work, functional ethylene receptors were thought to only be found in green plants. Here, we show that the cyanobacterium Synechocystis sp. PCC 6803 (Synechocystis) contains a functional ethylene receptor, SynEtr1. SynEtr1 contains a predicted ethylene binding domain, a photosensory cyanobacteriochrome (CBCR) domain, and a histidine kinase domain. We find SynEtr1 to display high affinity ethylene binding, and conserved residues from plant receptors are required for ethylene binding in SynEtr1. As a photoreceptor, SynEtr1 was previously reported to mediate phototaxis in Synechocystis. We show that ethylene regulates phototaxis via SynEtr1 by altering extracellular components of Synechocystis including type IV pili and extracellular polymeric substances (EPS). Both type IV pili and EPS are involved in many physiological processes, suggesting that the function of ethylene is not physiologically limited to phototaxis. We find that ethylene and SynEtr1 also affect cell sedimentation and biofilm formation. Thus, SynEtr1 functions as a bifunctional receptor mediating responses to both ethylene and light. This is the first known characterization of an ethylene receptor in a non-plant organism. Additionally, by scanning sequenced genomes, we discovered that putative ethylene receptors exist in many different species of both cyanobacteria and non-photosynthetic bacteria, indicating that ethylene may have a wide spread function throughout prokaryotes.