{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T04:31:23Z","timestamp":1790829083462,"version":"4.1.0"},"reference-count":73,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2019,8,20]],"date-time":"2019-08-20T00:00:00Z","timestamp":1566259200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["19-74-10100"],"award-info":[{"award-number":["19-74-10100"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["14-24-00020"],"award-info":[{"award-number":["14-24-00020"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>Systemic analysis of stress-induced transcription in the cyanobacterium Synechocystis sp. strain PCC 6803 identifies a number of genes as being induced in response to most abiotic stressors (heat, osmotic, saline, acid stress, strong light, and ultraviolet radiation). Genes for heat-shock proteins (HSPs) are activated by all these stresses and form a group that universally responds to all environmental changes. The functions of universal triggers of stress responses in cyanobacteria can be performed by reactive oxygen species (ROS), in particular H2O2, as well as changes in the redox potential of the components of the photosynthetic electron transport chain. The double mutant of Synechocystis sp. PCC 6803 (katG\/tpx, or sll1987\/sll0755), which is defective in antioxidant enzymes catalase (KatG) and thioredoxin peroxidase (Tpx), cannot grow in the presence of exogenous hydrogen peroxide (H2O2); and it is extremely sensitive to low concentrations of H2O2, especially under conditions of cold stress. Experiments on this mutant demonstrate that H2O2 is involved in regulation of gene expression that responds to a decrease in ambient temperature, and affects both the perception and the signal transduction of cold stress. In addition, they suggest that formation of ROS largely depends on the physical state of the membranes such as fluidity or viscosity. In cyanobacteria, an increase in membrane turnover leads to a decrease in the formation of ROS and an increase in resistance to cold stress. Therefore: (1) H2O2 is the universal trigger of stress responses in cyanobacterial cells; (2) ROS formation (in particular, H2O2) depends on the physical properties of both cytoplasmic and thylakoid membranes; (3) The destructive effect of H2O2 is reduced by increasing of fluidity of biological membranes.<\/jats:p>","DOI":"10.3390\/life9030067","type":"journal-article","created":{"date-parts":[[2019,8,21]],"date-time":"2019-08-21T11:19:06Z","timestamp":1566386346000},"page":"67","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":49,"title":["Universal Molecular Triggers of Stress Responses in Cyanobacterium Synechocystis"],"prefix":"10.3390","volume":"9","author":[{"given":"Kirill","family":"Mironov","sequence":"first","affiliation":[{"name":"Department of Molecular Biosystems, K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya street 35, 127276 Moscow, Russian"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9931-1762","authenticated-orcid":false,"given":"Maria","family":"Sinetova","sequence":"additional","affiliation":[{"name":"Department of Molecular Biosystems, K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya street 35, 127276 Moscow, Russian"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7916-462X","authenticated-orcid":false,"given":"Maria","family":"Shumskaya","sequence":"additional","affiliation":[{"name":"Department of Biology, School of Natural Sciences, Kean University, 1000 Morris Ave, Union, NJ 07083, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0142-7853","authenticated-orcid":false,"given":"Dmitry","family":"Los","sequence":"additional","affiliation":[{"name":"Department of Molecular Biosystems, K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya street 35, 127276 Moscow, Russian"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2386","DOI":"10.3390\/s100302386","article-title":"Stress sensors and signal transducers in cyanobacteria","volume":"10","author":"Los","year":"2010","journal-title":"Sensors"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"fnv090","DOI":"10.1093\/femsle\/fnv090","article-title":"Mechanosensitive ion channel MscL controls ionic fluxes during cold and heat stress in Synechocystis","volume":"362","author":"Bachin","year":"2015","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s11120-013-9823-4","article-title":"Regulatory role of membrane fluidity in gene expression and physiological functions","volume":"116","author":"Los","year":"2013","journal-title":"Photosynth. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"676","DOI":"10.3390\/life5010676","article-title":"Mechanisms of high temperature resistance of Synechocystis sp. PCC 6803: An impact of histidine kinase 34","volume":"5","author":"Sinetova","year":"2015","journal-title":"Life"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3254","DOI":"10.1039\/C6MB00551A","article-title":"Systemic analysis of transcriptomics of Synechocystis: Common stress genes and their universal triggers","volume":"12","author":"Sinetova","year":"2016","journal-title":"Mol. BioSyst."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1134\/S0026893316040117","article-title":"Lessons from cyanobacterial transcriptomics: Universal genes and triggers of stress responses","volume":"50","author":"Sinetova","year":"2016","journal-title":"Mol. Biol. (Moscow)"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1399-3054.2006.00608.x","article-title":"Histidine kinase Hik33 is an important participant in cold signal transduction in cyanobacteria","volume":"126","author":"Murata","year":"2006","journal-title":"Physiol. Plant."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1099\/mic.0.28510-0","article-title":"A putative sensor kinase, Hik31, is involved in the response of Synechocystis sp. strain PCC 6803 to the presence of glucose","volume":"152","author":"Kahlon","year":"2006","journal-title":"Microbiology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1128\/JB.06207-11","article-title":"Functions of the duplicated hik31 operons in central metabolism and responses to light, dark, and carbon sources in Synechocystis sp. strain PCC 6803","volume":"194","author":"Nagarajan","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/mmi.12442","article-title":"Essential role of the plasmid hik31 operon in regulating central metabolism in the dark in Synechocystis sp. PCC 6803","volume":"91","author":"Nagarajan","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1104\/pp.112.200659","article-title":"The CopRS two-component system is responsible for resistance to copper in the cyanobacterium Synechocystis sp. PCC 6803","volume":"159","author":"Reyes","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Giner-Lamia, J., L\u00f3pez-Maury, L., and Florencio, F.J. (2014). Global transcriptional profiles of the copper responses in the cyanobacterium Synechocystis sp. PCC 6803. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0108912"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1104\/pp.104.059097","article-title":"The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis","volume":"138","author":"Suzuki","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1111\/j.1365-313X.2006.02959.x","article-title":"Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803","volume":"49","author":"Kanesaki","year":"2007","journal-title":"Plant J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"12191","DOI":"10.1074\/jbc.M212204200","article-title":"Genetically-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis","volume":"278","author":"Inaba","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1039\/b903022k","article-title":"DNA supercoiling regulates the stress-inducible expression of genes in the cyanobacterium","volume":"5","author":"Prakash","year":"2009","journal-title":"Mol. BioSyst."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0014-5793(03)01188-8","article-title":"Antagonistic dark\/light-induced SigB\/SigD, group 2 sigma factors, expression through redox potential and their roles in cyanobacteria","volume":"554","author":"Imamura","year":"2003","journal-title":"FEBS Lett."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.febslet.2005.11.082","article-title":"The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC 6803","volume":"580","author":"Tuominen","year":"2006","journal-title":"FEBS Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"21531","DOI":"10.1074\/jbc.M412174200","article-title":"Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis","volume":"280","author":"Shumskaya","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1994","DOI":"10.1104\/pp.108.122713","article-title":"Characterization of single and double inactivation strains reveals new physiological roles for group 2 sigma factors in the cyanobacterium Synechocystis sp. PCC 6803","volume":"147","author":"Pollari","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"53078","DOI":"10.1074\/jbc.M410162200","article-title":"Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis","volume":"279","author":"Paithoonrangsarid","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3290","DOI":"10.1104\/pp.104.045047","article-title":"Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803","volume":"136","author":"Marin","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1111\/j.1574-6976.2010.00234.x","article-title":"Molecular biology of cyanobacterial salt acclimation","volume":"35","author":"Hagemann","year":"2011","journal-title":"FEMS Microbiol Rev."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1105\/tpc.13.4.793","article-title":"DNA microarray analysis of cyanobacterial gene expression during acclimation to high light","volume":"13","author":"Hihara","year":"2001","journal-title":"Plant Cell"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"6845","DOI":"10.1128\/JB.184.24.6845-6858.2002","article-title":"Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light","volume":"184","author":"Huang","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1128\/JB.185.5.1719-1725.2003","article-title":"DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803","volume":"185","author":"Hihara","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s11120-004-7761-x","article-title":"Identification of genes expressed in response to acid stress in Synechocystis sp. PCC 6803 using DNA microarrays","volume":"84","author":"Ohta","year":"2005","journal-title":"Photosynth. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1016\/j.bbabio.2012.03.028","article-title":"Slr0967 and Sll0939 induced by the SphR response regulator in Synechocystis sp. PCC 6803 are essential for growth under acid stress conditions","volume":"1817","author":"Uchiyama","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3882","DOI":"10.1128\/JB.186.12.3882-3888.2004","article-title":"Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: Negative and positive regulation and interactions between signal transduction pathways","volume":"186","author":"Hsiao","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1099\/mic.0.27530-0","article-title":"Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates osmostress-inducible gene expression","volume":"151","author":"Shapiguzov","year":"2005","journal-title":"Microbiology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.jphotobiol.2015.07.012","article-title":"Aquaporin-deficient mutant of Synechocystis is sensitive to salt and high-light stress","volume":"152","author":"Sinetova","year":"2015","journal-title":"J. Photochem. Photobiol. B. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1006\/bbrc.2001.6201","article-title":"Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803","volume":"290","author":"Kanesaki","year":"2002","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1046\/j.1365-2958.2001.02379.x","article-title":"Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis","volume":"40","author":"Suzuki","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2391","DOI":"10.1016\/j.bbagen.2016.07.006","article-title":"New insights in cyanobacterial cold stress responses: Genes, sensors, and molecular triggers","volume":"1860","author":"Sinetova","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1038\/nature13310","article-title":"Signal amplification and transduction in phytochrome photosensors","volume":"509","author":"Takala","year":"2014","journal-title":"Nature"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5739","DOI":"10.1074\/jbc.M311336200","article-title":"Alterations in global 5 patterns of gene expression in Synechocystis sp. PCC 6803 in response to 6 inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator","volume":"279","author":"Wang","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"7016","DOI":"10.1093\/nar\/gks382","article-title":"Sequence, structure and functional diversity of PD-(D\/E)XK phosphodiesterase superfamily","volume":"40","author":"Steczkiewicz","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3331","DOI":"10.1128\/JB.186.11.3331-3345.2004","article-title":"Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803","volume":"186","author":"Li","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2621","DOI":"10.1101\/gad.196741.112","article-title":"Rho and NusG suppress pervasive antisense transcription in Escherichia coli","volume":"26","author":"Peters","year":"2012","journal-title":"Genes Dev."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3793","DOI":"10.1093\/emboj\/18.13.3793","article-title":"SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA)","volume":"18","author":"Karzai","year":"1999","journal-title":"EMBO J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1016\/j.bbabio.2012.04.016","article-title":"RNA helicase, CrhR is indispensable for the energy redistribution and the regulation of photosystem stoichiometry at low temperature in Synechocystis sp. PCC6803","volume":"1817","author":"Sireesha","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_42","first-page":"1","article-title":"Inactivation of the RNA helicase CrhR impacts a specific subset of the transcriptome in the cyanobacterium Synechocystis sp. PCC 6803","volume":"24","author":"Georg","year":"2019","journal-title":"RNA Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0005-2760(98)00091-5","article-title":"Structure and expression of fatty acid desaturases","volume":"1394","author":"Los","year":"1998","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1046\/j.1365-2958.1997.5641912.x","article-title":"Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803","volume":"25","author":"Los","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2416","DOI":"10.1007\/s11434-010-3254-9","article-title":"Effects of a type-II RNA-binding protein on fatty acid composition in Synechocystis sp. PCC 6803","volume":"55","author":"Tang","year":"2010","journal-title":"Chin. Sci. Bull."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1074\/jbc.M008686200","article-title":"The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light","volume":"276","author":"He","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1016\/j.bbabio.2011.12.011","article-title":"Light-dependent cold-induced fatty acid unsaturation, changes in membrane fluidity, and alterations in gene expression in Synechocystis","volume":"1817","author":"Mironov","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1105\/tpc.114.124495","article-title":"A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC\/Alb3 insertase","volume":"26","author":"Chidgey","year":"2014","journal-title":"Plant Cell"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/s11120-007-9244-3","article-title":"Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with photosystem II","volume":"95","author":"Kufryk","year":"2008","journal-title":"Photosynth. Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"36758","DOI":"10.1074\/jbc.M606797200","article-title":"Photon flux density-dependent gene expression in Synechocystis sp. PCC 6803 is regulated by a small redox-responsive, LuxR-type regulator","volume":"281","author":"Nakamura","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1042\/BJ20100789","article-title":"The PedR transcriptional regulator interacts with thioredoxin to connect photosynthesis with gene expression in cyanobacteria","volume":"431","author":"Horiuchi","year":"2010","journal-title":"Biochem. J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1672","DOI":"10.1104\/pp.110.162990","article-title":"Essential role of glutathione in acclimation to environmental and redox perturbations in the cyanobacterium Synechocystis sp. PCC 6803","volume":"154","author":"Cameron","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1016\/j.bbabio.2014.02.005","article-title":"Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms","volume":"1837","author":"Schmitt","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1111\/j.0031-9317.2004.0232.x","article-title":"Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803","volume":"120","author":"Singh","year":"2004","journal-title":"Physiol. Plant."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1038\/nature04537","article-title":"The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation","volume":"440","author":"Lee","year":"2006","journal-title":"Nature"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1016\/j.bbalip.2016.01.003","article-title":"Sensing membrane thickness: Lessons learned from cold stress","volume":"1861","author":"Saita","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.jphotobiol.2014.03.001","article-title":"Cold-induced gene expression and \u03c93 fatty acid unsaturation is controlled by red light in Synechocystis","volume":"137","author":"Mironov","year":"2014","journal-title":"J. Photochem. Photobiol. B Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1038\/nsmb.1559","article-title":"Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride","volume":"16","author":"Guskov","year":"2009","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/s11120-017-0337-3","article-title":"Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria","volume":"133","author":"Maksimov","year":"2017","journal-title":"Photosynth. Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"6416","DOI":"10.1002\/j.1460-2075.1996.tb01033.x","article-title":"Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: Evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis","volume":"15","author":"Tasaka","year":"1996","journal-title":"EMBO J."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"4111","DOI":"10.1073\/pnas.1221194110","article-title":"Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light","volume":"110","author":"Allahverdiyeva","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1111\/tpj.14086","article-title":"Membrane physical state and stress regulation in Synechocystis: Fluidizing alcohols repress fatty acid desaturation","volume":"96","author":"Mironov","year":"2018","journal-title":"Plant J."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"9090","DOI":"10.1073\/pnas.90.19.9090","article-title":"The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803","volume":"90","author":"Vigh","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.plipres.2012.02.002","article-title":"Heat shock response in photosynthetic organisms: Membrane and lipid connections","volume":"51","author":"Glatz","year":"2012","journal-title":"Prog Lipid Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/S0014-5793(99)00309-9","article-title":"Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803","volume":"447","author":"Yamamoto","year":"1999","journal-title":"FEBS Lett."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1093\/pcp\/pcy067","article-title":"Hydrogen peroxide participates in perception and transduction of cold stress signal in Synechocystis","volume":"59","author":"Fedurayev","year":"2018","journal-title":"Plant Cell Physiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"6666","DOI":"10.1038\/s41598-018-25077-5","article-title":"Interaction of the GntR-family transcription factor Sll1961 with thioredoxin in the cyanobacterium Synechocystis sp. PCC 6803","volume":"8","author":"Kujirai","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1093\/pcp\/pcy221","article-title":"Group 2 sigma factors are central regulators of oxidative stress acclimation in cyanobacteria","volume":"60","author":"Hakkila","year":"2019","journal-title":"Plant Cell Physiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/j.redox.2014.02.006","article-title":"Hydrogen peroxide sensing, signaling and regulation of transcription factors","volume":"2","author":"Marinho","year":"2014","journal-title":"Redox Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1111\/j.1365-2958.2007.05836.x","article-title":"Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II","volume":"65","author":"Kojima","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"5860","DOI":"10.1074\/jbc.M115.706424","article-title":"Oxidation of a cysteine residue in elongation factor EF-Tu reversibly inhibits translation in the cyanobacterium Synechocystis sp. PCC 6803","volume":"291","author":"Yutthanasirikul","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"16555","DOI":"10.1073\/pnas.0806401105","article-title":"Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors","volume":"105","author":"Khursigara","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1146\/annurev-biochem-061516-044453","article-title":"Redox-based regulation of bacterial development and behavior","volume":"86","author":"Sporer","year":"2017","journal-title":"Annu. Rev. Biochem."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/9\/3\/67\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:12:30Z","timestamp":1760188350000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/9\/3\/67"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,20]]},"references-count":73,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2019,9]]}},"alternative-id":["life9030067"],"URL":"https:\/\/doi.org\/10.3390\/life9030067","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,20]]}}}