Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates osmostress-inducible gene expression

Shapiguzov, Alexey; Lyukevich, Alexander A.; Allakhverdiev, Suleyman I.; Sergeyenko, Tatiana V; Suzuki, Iwane; Murata, Norio; Los, Dmitry A.

doi:10.1099/mic.0.27530-0

Cited by 48 publications

(57 citation statements)

References 27 publications

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“…1B), indicating that osmoregulation capacity was exceeded, and cells were no longer able to uphold turgor, and began to leak and shrink when the salinity became too high. The reduction in cell size in response to osmotic stress is known as plasmolysis, and is also widely reported for other bacteria (Koch 1984, Csonka 1989, Shapiguzov et al 2005. The combination of leakage and cell lysis most likely resulted in the high extracellular microcystin concentrations observed at salinities exceeding 10 g l -1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa

Tonk¹,

Bosch²,

Visser³

et al. 2007

Aquat. Microb. Ecol.

167

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Section: Discussionmentioning

confidence: 99%

Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa

Tonk¹,

Bosch²,

Visser³

et al. 2007

Aquat. Microb. Ecol.

167

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“…Salt acclimation in cyanobacteria occurs in five phases (Hagemann, 2011). A salt shock causes rapid shrinking of the cells due to loss of water (Blumwald et al, 1983) via aquaporins (Shapiguzov et al, 2005). In the second phase, ions including Na + and Cl 2 passively enter the cells and water flows back to the cells (Reed et al, 1985) but cellular processes including photosynthesis (Allakhverdiev et al, 2000) and gene expression (Hagemann et al, 1994;Fulda et al, 2006) remain slow due to high ion (especially Na + ) content of the cells.…”

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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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“…Water flux occurs mainly through water-permeable channels, including aquaporins, simultaneously with the transport of ions across the membrane and the change in concentration of the compatible solutes synthesized de novo in the cells. In Synechocystis, it has been reported that very little shrinkage of ⌬aqpZ cells was observed after addition of large amounts of a nonionic compound, sorbitol, to the medium (7,42). Unlike Na ϩ , sorbitol shows very low permeation across the plasma membrane in the cyanobacterium Synechococcus sp.…”

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confidence: 99%

“…Simultaneously with the transport of ions across the membrane or the change in intracellular concentration of compatible solutes, such as glucosylglycerol, carbamides, polyols, purines, pyrimidines, and glycerol, by de novo synthesis in response to the external salt concentration or osmolarity change, water flux occurs mainly through water-permeable channels called aquaporins (18,19,31,32,39,40,44,47). Synechocystis contains in its genome a single-copy gene encoding an aquaporin homolog, aqpZ (1,7,42). The AqpZ protein resides in the plasma membrane in the cell (1).…”

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confidence: 99%

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Aquaporin AqpZ Is Involved in Cell Volume Regulation and Sensitivity to Osmotic Stress in Synechocystis sp. Strain PCC 6803

et al. 2012

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The moderately halotolerant cyanobacterium Synechocystis sp. strain PCC 6803 contains a plasma membrane aquaporin, AqpZ. We previously reported that AqpZ plays a role in glucose metabolism under photomixotrophic growth conditions, suggesting involvement of AqpZ in cytosolic osmolarity homeostasis. To further elucidate the physiological role of AqpZ, we have studied its gene expression profile and its function in Synechocystis. The expression level of aqpZ was regulated by the circadian clock. AqpZ activity was insensitive to mercury in Xenopus oocytes and in Synechocystis, indicating that the AqpZ can be categorized as a mercury-insensitive aquaporin. Stopped-flow light-scattering spectrophotometry showed that addition of sorbitol and NaCl led to a slower decrease in cell volume of the Synechocystis ⌬aqpZ strain than the wild type. The ⌬aqpZ cells were more tolerant to hyperosmotic shock by sorbitol than the wild type. Consistent with this, recovery of oxygen evolution after a hyperosmotic shock by sorbitol was faster in the ⌬aqpZ strain than in the wild type. In contrast, NaCl stress had only a small effect on oxygen evolution. The amount of AqpZ protein remained unchanged by the addition of sorbitol but decreased after addition of NaCl. This decrease is likely to be a mechanism to alleviate the effects of high salinity on the cells. Our results indicate that Synechocystis AqpZ functions as a water transport system that responds to daily oscillations of intracellular osmolarity.

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Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates osmostress-inducible gene expression

Cited by 48 publications

References 27 publications

Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa

Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa

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

Aquaporin AqpZ Is Involved in Cell Volume Regulation and Sensitivity to Osmotic Stress in Synechocystis sp. Strain PCC 6803

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