Phototactic signaling network in rod-shaped cyanobacteria: A study on Synechococcus elongatus UTEX 3055.

Abstract

Light-controlled motility is advantageous for photosynthetic prokaryotes to better survive in environment with constantly changing light conditions. For cyanobacteria, light is both an energy source for photosynthesis and a stress factor. Consequently, some cyanobacteria evolved the ability to control type-IV pili (T4P)-mediated surface motility using a chemotaxis-like system in response to light signals. Extensive studies on the mechanism of phototaxis has been conducted in the spherical Synechocystis sp. PCC 6803 and the filamentous strain Nostoc punctiforme, while less is explored in rod-shaped cyanobacteria such as Synechococcus species. In this study, we investigated the phototaxis pathway in the unicellular rod-shaped cyanobacterium Synechococcus elongatus UTEX 3055, which exhibits bidirectional phototaxis using a single tax1 operon, in contrast to more complex and multiple gene clusters revealed in Synechocystis sp. PCC 6803. Results obtained by protein-protein interaction assays and protein subcellular localization experiments indicated that proteins encoded by the tax1 operon form large clusters that asymmetrically distributed both between the two poles and within the same pole. In vitro phosphorylation assays and site-directed mutations of conserved phosphorylation sites in PixL_Se, PixG_Se and PixH_Se demonstrate that PixL_Se acts as a histidine kinase, and PixG_Se and PixH_Se as response regulators for signal transduction. We further show that PixG_Se and PixH_Se are recruited to cell poles via interactions with the N-terminal region of PixL_Se. While phosphotransfer reactions in this signaling pathway are critical for phototactic signaling, the two response regulators appear to play different roles in the control of phototaxis. This study provides a framework for further investigation into the complex phototactic signaling network in rod-shaped cyanobacteria with clearly defined cell poles in contrast to round shaped Synechocystis species with virtual cells poles through light-lensing effect.