Stress Signaling in Cyanobacteria: A Mechanistic Overview

Abstract

Cyanobacteria are highly diverse, widely distributed photosynthetic bacteria inhabiting various environments ranging from deserts to the cryosphere. Throughout this range of niches, they have to cope with various stresses and kinds of deprivation which threaten their growth and viability. In order to adapt to these stresses and survive, they have developed several global adaptive responses which modulate the patterns of gene expression and the cellular functions at work. Sigma factors, two-component systems, transcriptional regulators and small regulatory RNAs acting either separately or collectively, for example, induce appropriate cyanobacterial stress responses. The aim of this review is to summarize our current knowledge about the diversity of the sensors and regulators involved in the perception and transduction of light, oxidative and thermal stresses, and nutrient starvation responses. The studies discussed here point to the fact that various stresses affecting the photosynthetic capacity are transduced by common mechanisms.

Keywords: cyanobacteria; gene expression; signaling; stress.

Figure 1

Regulation of high light stress acclimation.

Figure 2

Regulation of oxidative stress responses. (A)Superoxide anion stress. In the absence of stress, the PrqR sensor might phosphorylate the response regulator CalA, which therefore represses the gene transcription process. In the presence of superoxide, PrqR is inactivated by a hitherto unknown mechanism. The Group 2 sigma factors SigB and/or SigD associate(s) with the RNA polymerase, resulting in the initiation of the transcription process. (B) Peroxide stress. The metalloregulator PerR represses gene transcription in the absence of peroxide. Under oxidative conditions, metal catalyzed oxidation (MCO) inactivates PerR, thus inducing gene transcription.

Figure 3

Regulation of salt stress responses. (A) the transcription of the spsA gene involved in the synthesis of sucrose is repressed by RpaB. The cognate sensor involved has not yet been identified. (B) the transcription of the ggpS gene involved in the synthesis of glycosylglycerol is subjected to the negative control of GgpR and LexA. Under salt stress conditions, the presence of the SigF sigma factor enables the RNA polymerase to initiate the transcription process. The dephosphorylation of LexA inhibits its action. The mechanism underlying GgpR inhibition is not known.

Figure 4

Heat shock response regulation. Under optimal growth conditions, the transcription of the hsp genes is repressed by HrcA, which binds to a conserved sequence called CIRCE. Upon undergoing heat shock, HrcA is inactivated and hsp transcription is induced. The GroEL chaperone facilitates the refolding of HrcA at the release of the stress, thus acting as the molecular sensor of the signal. Some of the hsp mRNAs carry an untranslated sequence forming a secondary (thermometer) structure sequestering the ribosome binding site under normal growth temperature conditions. Upon undergoing heat shock, this secondary structure dissociates, which makes it possible for the translation process to proceed.

Figure 5

Regulation of carbon and nitrogen acclimations. (A) Low carbon response. NdhR (CcmR) is the main transcriptional regulator of the low carbon response. The activity of NdhR is submitted to a dual allosteric regulation where 2-OG and NAD⁺ act as co-activators and 2-PG as co-repressor. When inorganic carbon level is sufficient, the carboxylase activity of Rubisco is advantaged and 2-PG concentration is low. The levels of 2-OG and NAD⁺ are high, and NdhR is active and represses the transcription of target genes. Under carbon starvation, the oxygenase activity of Rubisco generates 2-PG that binds to NdhR and inhibits its activity, leading to the induction of CO₂ concentrating mechanism (CCM). The cmp operon, which is also part of CCM, is under the positive control of CmpR. 2-PG and RuBP (1,5 ribulose biphosphate, blue dot) act as co-activators of CmpR. 2-PG and RubP are generated by the oxygenase activity of RubisCo under low carbon conditions. The low carbon response is also regulated by LexA and AbrB and submitted to post-transcriptional regulations (see text for details). (B) Nitrogen starvation. The NtcA protein, the main transcriptional factor of nitrogen-induced genes, is activated by PipX. The intracellular level of 2-OG (red circles), which reflects the nitrogen status of the cell, is perceived by PII and NtcA. Under replete nitrogen conditions, the 2-OG level is low, PipX interacts with PII, and NtcA is inactive. When nitrogen is a limiting factor, 2-OG accumulates, and PipX changes its partner and interacts with NtcA. The 2-OG-NtcA-PipX complex regulates the gene transcription process. The post-transcriptional regulation mechanisms involved in nitrogen starvation signaling are not presented in the figure.

Figure 6

Regulation of phosphate and iron acclimations. (A) Phosphate starvation. The group of genes induced in response to phosphate starvation is called “the pho regulon”. In response to phosphate limitation, the transcription of these genes is activated by the TCS formed by the kinase SphS and the response regulator SphR. Under replete phosphate conditions, the activity of SphS is inhibited by the protein SphU, presumably by interacting with the transmitter domain of SphS. (B) Iron starvation. The Fur repressor is a metalloprotein in which iron serves as a cofactor. When iron becomes limited, it is inactivated by the shift of Fur to its apoform, and the transcription process is thus induced. In addition, the translation of several genes is inhibited by the sRNA isaR1, which is expressed under iron starvation conditions.