The Histidine Kinase Hik34 Is Involved in Thermotolerance by Regulating the Expression of Heat Shock Genes in Synechocystis

Suzuki, Iwane; Kanesaki, Yu; Hayashi, Hidenori; Hall, John J.; Simon, William J.; Slabas, Antoni R.; Murata, Norio

doi:10.1104/pp.104.059097

Cited by 93 publications

(92 citation statements)

References 46 publications

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“…The genes reported to be under the control of the Hik34-Rre1 pair following hyperosmotic or salt stress are rather general stress response genes; this may explain why the authors could not identify the sensor partner upstream of Hik34 in the regulatory pathway. In agreement with their previous data, the same group recently showed that Hik34 is required for thermotolerance (probably by regulating the expression of some heat shock genes) and that the purified protein could autophosphorylate in vitro (134). There do not appear to be any proteins orthologous to this Chk34 group in any of the other 110 completed bacterial genome sequences.…”

Section: Histidine Kinasessupporting

confidence: 69%

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Cyanobacterial Two-Component Proteins: Structure,Diversity, Distribution, andEvolution

Ashby

Houmard

2006

Microbiol Mol Biol Rev

125

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SUMMARY A survey of the already characterized and potential two-component protein sequences that exist in the nine complete and seven partially annotated cyanobacterial genome sequences available (as of May 2005) showed that the cyanobacteria possess a much larger repertoire of such proteins than most other bacteria. By analysis of the domain structure of the 1,171 potential histidine kinases, response regulators, and hybrid kinases, many various arrangements of about thirty different modules could be distinguished. The number of two-component proteins is related in part to genome size but also to the variety of physiological properties and ecophysiologies of the different strains. Groups of orthologues were defined, only a few of which have representatives with known physiological functions. Based on comparisons with the proposed phylogenetic relationships between the strains, the orthology groups show that (i) a few genes, some of them clustered on the genome, have been conserved by all species, suggesting their very ancient origin and an essential role for the corresponding proteins, and (ii) duplications, fusions, gene losses, insertions, and deletions, as well as domain shuffling, occurred during evolution, leading to the extant repertoire. These mechanisms are put in perspective with the different genetic properties that cyanobacteria have to achieve genome plasticity. This review is designed to serve as a basis for orienting further research aimed at defining the most ancient regulatory mechanisms and understanding how evolution worked to select and keep the most appropriate systems for cyanobacteria to develop in the quite different environments that they have successfully colonized.

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Section: Histidine Kinasessupporting

confidence: 69%

“…Quite interestingly, this Chk34 protein was also shown to be essential for thermotolerance in Synechocystis sp. strain PCC 6803, possibly by negatively regulating the expression of certain heat shock genes (134). It is thus likely a quite important protein for cyanobacteria.…”

Section: Hks and Rrs Common To All Genomesmentioning

confidence: 99%

Cyanobacterial Two-Component Proteins: Structure,Diversity, Distribution, andEvolution

Ashby

Houmard

2006

Microbiol Mol Biol Rev

125

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“…The Synechocystis genome contains 47 genes that encode putative histidine kinases, and 45 genes that encode putative response regulators (Los et al, 2008). In Synechocystis, characterization of gene-interruption mutants has identified histidine kinases involved in sensing environmental stimuli, including high light, cold and oxidative stress (Hik33), heat (Hik34), salt stress and hyperosmotic stress (Hik33, Hik34, Hik2, Hik41, Hik16 and Hik10), and phosphate limitation (Hik7) (Hirani et al, 2001;Hsiao et al, 2004;Kanesaki et al, 2007;Mikami et al, 2002;Paithoonrangsarid et al, 2004;Shoumskaya et al, 2005;Suzuki et al, 2005). These data demonstrate that one histidine kinase may respond to more than one type of stimulus and that multiple histidine kinases may respond to any specific environmental cue.…”

Section: Introductionmentioning

confidence: 99%

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

2011

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We have investigated the response of the cyanobacterium Synechocystis sp. PCC 6803 during growth at very low O 2 concentration (bubbled with 99.9 % N 2 /0.1 % CO 2 ). Significant transcriptional changes upon low-O 2 incubation included upregulation of a cluster of genes that contained psbA1 and an operon that includes a gene encoding the two-component regulatory histidine kinase, Hik31. This regulatory cluster is of particular interest, since there are virtually identical copies on both the chromosome and plasmid pSYSX. We used a knockout mutant lacking the chromosomal copy of hik31 and studied differential transcription during the aerobiclow-O 2 transition in this DHik31 strain and the wild-type. We observed two distinct responses to this transition, one Hik31 dependent, the other Hik31 independent. The Hik31-independent responses included the psbA1 induction and genes involved in chlorophyll biosynthesis. In addition, there were changes in a number of genes that may be involved in assembling or stabilizing photosystem (PS)II, and the hox operon and the LexA-like protein (Sll1626) were upregulated during low-O 2 growth. This family of responses mostly focused on PSII and overall redox control. There was also a large set of genes that responded differently in the absence of the chromosomal Hik31. In the vast majority of these cases, Hik31 functioned as a repressor and transcription was enhanced when Hik31 was deleted. Genes in this category encoded both core and peripheral proteins for PSI and PSII, the main phycobilisome proteins, chaperones, the ATP synthase cluster and virtually all of the ribosomal proteins. These findings, coupled with the fact that DHik31 grew better than the wild-type under low-O 2 conditions, suggested that Hik31 helps to regulate growth and overall cellular homeostasis. We detected changes in the transcription of other regulatory genes that may compensate for the loss of Hik31. We conclude that Hik31 regulates an important series of genes that relate to energy production and growth and that help to determine how Synechocystis responds to changes in O 2 conditions.

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“…In Synechocystis, transcriptome analyses with His kinase/response regulator mutants have revealed that at least Hik33/Rre31, Hik34/Rre1, Hik2/Rre1, Hik16/Hik41/Rre17, and Hik10/Rre3 participate, but any of these regulators could be inactivated without great impact on growth in salt stress conditions, suggesting functional redundancy (Shoumskaya et al, 2005). Furthermore, these regulators are involved in other stresses like osmotic, oxidative, or heat stress (Paithoonrangsarid et al, 2004;Shoumskaya et al, 2005;Suzuki et al, 2005;Kanesaki et al, 2007).…”

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confidence: 99%

The SigB σ Factor Regulates Multiple Salt Acclimation Responses of the Cyanobacterium Synechocystis sp. PCC 6803

et al. 2011

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Changing of principal s factor in RNA polymerase holoenzyme to a group 2 s factor redirects transcription when cyanobacteria acclimate to suboptimal environmental conditions. The group 2 sigma factor SigB was found to be important for the growth of the cyanobacterium Synechocystis sp. PCC 6803 in high-salt (0.7 M NaCl) stress but not in mild heat stress at 43°C although the expression of the sigB gene was similarly highly, but only transiently up-regulated at both conditions. The SigB factor was found to regulate many salt acclimation processes. The amount of glucosylglycerol-phosphate synthase, a key enzyme in the production of the compatible solute glucosylglycerol, was lower in the inactivation strain DsigB than in the control strain. Addition of the compatible solute trehalose almost completely restored the growth of the DsigB strain at 0.7 M NaCl. High-salt conditions lowered the chlorophyll and phycobilin contents of the cells while protective carotenoid pigments, especially zeaxanthin and myxoxanthophyll, were up-regulated in the control strain. These carotenoids were up-regulated in the DsigCDE strain (SigB is the only functional group 2 s factor) and down-regulated in the DsigB strain under standard conditions. In addition, the HspA heat shock protein was less abundant and more abundant in the DsigB and DsigCDE strains, respectively, than in the control strain in high-salt conditions. Some cellular responses are common to heat and salt stresses, but pretreatment with mild heat did not protect cells against salt shock although protection against heat shock was evident.

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The Histidine Kinase Hik34 Is Involved in Thermotolerance by Regulating the Expression of Heat Shock Genes in Synechocystis

Cited by 93 publications

References 46 publications

Cyanobacterial Two-Component Proteins: Structure,Diversity, Distribution, andEvolution

Cyanobacterial Two-Component Proteins: Structure,Diversity, Distribution, andEvolution

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

The SigB σ Factor Regulates Multiple Salt Acclimation Responses of the Cyanobacterium Synechocystis sp. PCC 6803

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