Stress sensors and signal transducers in cyanobacteria

Abstract

In living cells, the perception of environmental stress and the subsequent transduction of stress signals are primary events in the acclimation to changes in the environment. Some molecular sensors and transducers of environmental stress cannot be identified by traditional and conventional methods. Based on genomic information, a systematic approach has been applied to the solution of this problem in cyanobacteria, involving mutagenesis of potential sensors and signal transducers in combination with DNA microarray analyses for the genome-wide expression of genes. Forty-five genes for the histidine kinases (Hiks), 12 genes for serine-threonine protein kinases (Spks), 42 genes for response regulators (Rres), seven genes for RNA polymerase sigma factors, and nearly 70 genes for transcription factors have been successfully inactivated by targeted mutagenesis in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Screening of mutant libraries by genome-wide DNA microarray analysis under various stress and non-stress conditions has allowed identification of proteins that perceive and transduce signals of environmental stress. Here we summarize recent progress in the identification of sensory and regulatory systems, including Hiks, Rres, Spks, sigma factors, transcription factors, and the role of genomic DNA supercoiling in the regulation of the responses of cyanobacterial cells to various types of stress.

Keywords: histidine kinase; response regulator; sensor; serine-threonine kinase; stress; supercoiling; transducer.

Figure 1.

A general scheme showing the responses of a cyanobacterial cell to environmental stress. Adopted from [28]. Published with permission of Horizon Scientific Press / Caister Academic Press.

Figure 2.

Schematic representation of positive (A) and negative (B) modes regulation of stress-inducible expression of genes. Solid arrows indicate signals that activate downstream components and dotted arrows indicate their absence. The inverted ‘T’ indicates signals that repress the expression of downstream genes. Red arrows correspond to the enhancement of gene expression. Adopted from [28]. Published with permission of Horizon Scientific Press / Caister Academic Press.

Figure 3.

Schematic presentation of two-component system Hik33-Rre26 involved in the transduction of low-temperature stress. Primary signals are represented by open blue arrows. The sensory histidine kinase Hik33 supposedly perceives the temperature-induced rigidification in the cytoplasmic membrane. It tranduces the phosphoryl group to the response regulator Rre26, which itself might bind to promoter region of the genes to induce their transcription. Uncharacterized mechanisms are represented by question marks. Genes with induction factors (ratios of transcript levels of stressed cells to those of non-stressed cells) higher than 3:1 are included in these scheme. Adopted from [28]. Published with permission of Horizon Scientific Press / Caister Academic Press.

Figure 4.

Schematic representation of the monomeric Hik33 of Synechocystis sp. PCC 6803 and its homologs from other organisms: 7942–Synechococcus elongatus PCC7942; MIT9301–Prochlorococcus strain MIT 9301; P. purpurea–Porphyra purpurea; B.s.–Bacillus subtilis. Numbers along the polypeptide sequences represent the corresponding numbers of amino acids starting from the first methionine. HAMP, PAS, PAC, HisKA, HATPase_c–the characteristic domains found by SMART software (http://smart.embl-heidelberg.de/). Hepcidin antimicrobial peptide (HAMP), HAMP-linker domains; LZ, leucine zipper domains; PER-ARNT-SIM (PAS), PAS domains that contain the amino acid motifs Per, Arnt, Sim and phytochrome [36]; blue rods represent the transmembrane domains.

Figure 5.

Hypothetical schemes of two-component systems that are involved in the transduction of salt stress (A) and hyperosmotic stress (B), as well as the genes that are under the control of the individual two-component systems. Primary signals are represented by open arrows. Hiks that posess transmembrane domains are indicated as ellipses (Hik33, Hik16, Hik10); Hik33 is in a red ellipse; soluble Hiks are shown as horizontal boxes (Hik34, Hik2, Hik41); Rres are indicated as hexagons, and selectively regulated genes are shown in vertical boxes. Uncharacterized mechanisms are represented by question marks. Genes with induction factors higher than 4.0 are included in these schemes. Adopted from [28]. Published with permission of Horizon Scientific Press / Caister Academic Press.

Figure 6.

Hypothetical model for the sensing of Mn²⁺ ions, the transduction of the Mn²⁺ signal, and the regulation of expression of the mntCAB eperon that encodes the Mn²⁺ transporter. His and Asp residues that might be involved in a phosphorelay are indicated by the encircled H and D, respectively. Adopted from [73].

Figure 7.

Transcription factors of Synechocystis classified according to the specific architecture of their DNA-binding domais. WH-“Winged helix” DNA-binding domain; C-term-C-terminal effector domain of the bipartite response regulators; Abr-AbrB/MazE/MraZ-like domain; Putative-Putative DNA-binding domain; IHF-IHF-like DNA-binding proteins; HD-Homeodomain-like; TRP-TrpR-like; Pbp-Periplasmic binding protein-like II; GAF-GAF domain; cAMP-cAMP-binding domain-like; Lex-LexA/Signal peptidase; MM-Precorrin-8X metylmutase; P-P-loop containing nucleotide triphosphate hydrolases; TetR-Tetracyclin repressor-like, C-terminal domain; CheY-CheY-like domain.

Figure 8.

A scheme of the perception and transduction of cold-stress signals by cyanobacterial cells. The sensory histidine kinase Hik33 perceives the temperature-induced rigidification in the cytoplasmic membrane. Upon autophosphorylation of the Hik33 dimer, it tranduces the phosphoryl group to the response regulator Rre26, which binds to promoter region of the genes to induce their transcription. The Hik33-Rre26 two-component sensor and transduction system regulates a part of cold-inducible genes. This part, however, is also under control of the cold-induced increase in negative supercoiling of the genomic DNA. The latter mechanism controls cold-induced transcription of genes for RNA chaperons, translation, cell wall metabolism, and regulation of the membrane fluidity.