Control of light-dependent behaviour in cyanobacteria by the second messenger cyclic di-GMP

Abstract

Nucleotide-derived signalling molecules control a wide range of cellular processes in all organisms. The bacteria-specific cyclic dinucleotide c-di-GMP plays a crucial role in regulating motility-to-sessility transitions, cell cycle progression, and virulence. Cyanobacteria are phototrophic prokaryotes that perform oxygenic photosynthesis and are widespread microorganisms that colonize almost all habitats on Earth. In contrast to photosynthetic processes that are well understood, the behavioural responses of cyanobacteria have rarely been studied in detail. Analyses of cyanobacterial genomes have revealed that they encode a large number of proteins that are potentially involved in the synthesis and degradation of c-di-GMP. Recent studies have demonstrated that c-di-GMP coordinates many different aspects of the cyanobacterial lifestyle, mostly in a light-dependent manner. In this review, we focus on the current knowledge of light-regulated c-di-GMP signalling systems in cyanobacteria. Specifically, we highlight the progress made in understanding the most prominent behavioural responses of the model cyanobacterial strains Thermosynechococcus vulcanus and Synechocystis sp. PCC 6803. We discuss why and how cyanobacteria extract crucial information from their light environment to regulate ecophysiologically important cellular responses. Finally, we emphasize the questions that remain to be addressed.

Keywords: c-di-GMP; cyanobacteria; light-dependent behaviour; second messenger signalling.

Figure 1.

Regulation of cellular behaviour by c-di-GMP in cyanobacteria. Light, especially blue light, controls many c-di-GMP-dependent lifestyle decisions in cyanobacteria. However, other external factors might contribute to c-di-GMP-dependent regulation. In Synechocystis (coccoid bacteria), blue light leads to an overall increase in the cellular c-di-GMP concentration, which induces flocculation and biofilm formation and inhibits motility. A high c-di-GMP concentration leads to cellulose-dependent aggregation of T. vulcanus (a rod-shaped bacterium). C-di-GMP influences phototaxis reversals of T. vulcanus and heterocyst development in the filamentous cyanobacterium Anabaena sp. PCC 7120.

Figure 2.

The role of c-di-GMP in Synechocystis behaviour. The C-terminal blue/green light photosensory module of Cph2 inhibits motility under blue light by generation of the second messenger c-di-GMP. The N-terminal red/far-red dependent phytochrome module of Cph2 harbours an active EAL domain and an inactive GGDEF domain. Cip1 is an active diguanylate cyclase that interacts with Cph2. C-di-GMP controls gene expression. The major targets are genes encoding minor pilins, which are potential components of type IV pili. Several of these minor pilins control different functions of type IV pili, including motility, flocculation, and natural competence.

Figure 3.

The role of c-di-GMP in T. vulcanus behaviour. Three CBCRs regulate c-di-GMP signalling. Blue light induces cyclic di-GMP formation, whereas teal and green light lead to c-di-GMP degradation. The cellulose synthase XcsA is activated by c-di-GMP and supports the aggregation of T. vulcanus cells. The effector for c-di-GMP-dependent phototaxis reversals is unknown.