Moving toward Light in Response to a Gas: A Novel Cyanobacterial Ethylene Receptor

It has been generally thought that the gaseous hormone ethylene is sensed solely by plants and a few algae, but in this issue, Lacey and Binder (2016) demonstrate that a cyanobacterium can sense and respond to ethylene. The plant ethylene receptor is derived from the two-component His kinase receptor family, which is prevalent in prokaryotes (Chang et al., 1993). Interestingly, ethylene receptor homologs have been observed in some prokaryotes—particularly cyanobacteria—but not in other eukaryotes (Mount and Chang, 2002; Wang et al., 2006; Lacey and Binder, 2016), suggesting that plants acquired the ethylene receptor through horizontal gene transfer following endosymbiosis of an ancestral cyanobacterium that became the chloroplast more than 1 billion years ago (Mount and Chang, 2002). Despite evidence that several extant cyanobacteria can bind ethylene (Rodríguez et al., 1999; Wang et al., 2006), the significance of this had been unexplored, and the function of prokaryotic ethylene receptor homologs had never, to our knowledge, been determined. Moreover, nearly 2 decades ago, a cyanobacterial homolog, Synechocystis Ethylene response1 (SynEtr1 or slr1212), was found to be involved in binding ethylene in Synechocystis (Synechocystis sp. PCC 6803; Rodríguez et al., 1999). This led to years of speculation concerning whether SynEtr1 is indeed an ethylene receptor, and if so, what the functional role of ethylene is in this cyanobacterium.

Now, Lacey and Binder (2016) have elegantly demonstrated that SynEtr1 binds ethylene and operates as a receptor in Synechocystis. Like plant ethylene receptors, SynEtr1 is a two-component His kinase that contains a conserved N-terminal transmembrane ethylene-binding domain and a C-terminal His kinase domain. SynEtr1 is different from plant ethylene receptors in that it has a conserved phytochrome-like light-sensing domain (Ulijasz et al., 2009), which was previously shown to sense light and regulate phototactic mobility (Narikawa et al., 2011; Song et al., 2011). Lacey and Binder (2016) have now linked this light-sensing response with ethylene binding, revealing that Synechocystis responds to externally applied ethylene by an enhanced phototactic migration toward light. Thus, SynEtr1 is a dual receptor for ethylene and light. A mutant carrying an insertion in the ethylene-binding domain confers an even stronger phototactic response. Based on their findings, Lacey and Binder (2016) propose that SynEtr1 operates as an inverse-agonist receptor (similar to the plant ethylene receptor) by reducing phototaxis, while ethylene inhibits this negative regulation, thus stimulating phototaxis. Lacey and Binder (2016) also find that ethylene slightly increases the amount of pili and enhances biofilm formation, and that the insertion mutant exhibits a large increase in the number of pili and a reduction in static sedimentation, both of which are linked to the phototactic response.

Because Synechocystis lacks machinery known to synthesize ethylene, the cyanobacterial receptor probably perceives ethylene originating from the environment, highlighting the underestimated importance of ethylene as an environmental signal. As Lacey and Binder (2016) discuss, there are several interesting possibilities concerning the ecophysiological roles that ethylene and light integration could play in Synechocystis and other prokaryotes.