Ethylene causes transcriptomic changes in Synechocystis during phototaxis

Abstract

Ethylene is well known as a plant hormone, but its role in bacteria is poorly studied.We recently showed that Synechocystis sp. Strain PCC 6803 has a functional receptor for ethylene, ethylene response 1 (Etr1), that is involved in various processes such as phototaxis in response to directional light and biofilm formation. Here, we use RNA sequencing to examine the changes in gene transcripts caused by ethylene under phototaxis conditions. Over 500 gene transcripts across many functional categories, of approximately 3700 protein-encoding genes, were altered by application of ethylene. In general, ethylene caused both up-and downregulation of genes within a functional category. However, the transcript levels of amino acid metabolism genes were mainly upregulated and cell envelope genes were mostly downregulated by ethylene. The changes in cell envelope genes correlate with our prior observation that ethylene affects cell surface properties to alter cell motility. Ethylene caused a twofold or more change in 62 transcripts with the largest category of upregulated genes annotated as transporters and the largest category of downregulated genes annotated as glycosyltransferases which sometimes are involved in changing the composition of sugars on the cell surface. Consistent with changes in cell envelope, glycosyltransferase, and transporter gene transcripts, application of ethylene altered the levels of specific sugar moieties on the surface of cells. Light signaling from Etr1 involves two proteins (Slr1213 and Slr1214) and a small, noncoding RNA, carbon stress-induced RNA1 (csiR1). Application of ethylene caused a rapid, but transient, decrease in the transcript levels of etr1, slr1213, and slr1214 and a rapid and prolonged decrease in csiR1 transcript. Deletion of Slr1214 caused a large increase in csiR1 transcript levels and ethylene lowered csiR1 transcript.These data combined with prior reports indicate that ethylene functions as a signal to affect a variety of processes altering the physiology of Synechocystis cells. K E Y W O R D Sethylene receptor, extracellular polymeric substances, RNA-seq, Synechocystis

Ethylene Receptors in Nonplant Species

“…[51] In Synechocystis, these traits are controlled by type IV pili and extracellular polymeric substance (EPS). [52][53][54][55] Interestingly, ethylene affects the levels of pilin proteins and increases the number of type IV pili synthesized, and, alters the sugar composition of the EPS [42,56] suggesting that ethylene affects these physiological traits by changing type IV pili and EPS composition. Application of ethylene also causes a small increase in photosystem II levels with a parallel increase in growth rate of about 20%, [42,57] but these effects do not explain the much larger effects that ethylene has on the other physiological traits mentioned above.…”

“…One showed that the fatty acid composition of the membranes was altered by ethylene [57] and another showed that application of ethylene to phototaxing cells caused wide-spread alterations in gene transcription causing altered mRNA levels for over 500 genes. [56] Additionally, ethylene causes a down regulation of several genes in the genomic region of SynEtr1 including CsiR1 (for Carbon stress inducted RNA1), slr1214, and slr1215. [56] These will be discussed more in the next section.…”

“…[56] Additionally, ethylene causes a down regulation of several genes in the genomic region of SynEtr1 including CsiR1 (for Carbon stress inducted RNA1), slr1214, and slr1215. [56] These will be discussed more in the next section.…”

“…Where studied, these effects of ethylene are eliminated when SynEtr1 is deleted (ΔSynEtr1) [42,56,57] indicating that SynEtr1 is a bona fide receptor for ethylene. An interesting observation is that ΔSynEtr1 cells move farther in response to light, show enhanced biofilm formation, and contain an increased number of type IV pili; these changes are reversed when the ΔSynEtr1 cells are complemented with SynEtr1 but not a mutant SynEtr1 that cannot bind ethylene.…”

“…By contrast, ethylene appears to inhibit this process ( Figure 1). While the effect of ethylene on SynEtr1 autophosphorylation and phosphorelay have not been examined, treatment of Synechocystis cells with ethylene results in a rapid decrease in the transcript levels of CsiR1 and slr1214 [56] which is in contrast to the effects of light. Deletion of slr1214 causes the cells to be insensitive to ethylene [42] supporting the idea that it is also part of the ethylene signaling pathway in addition to its role in light sensing.…”