Abstract
Membrane fluidity is the important regulator of cellular responses to changing ambient temperature. Bacteria perceive cold by the transmembrane histidine kinases that sense changes in thickness of the cytoplasmic membrane due to its rigidification. In the cyanobacterium Synechocystis, about a half of cold-responsive genes is controlled by the light-dependent transmembrane histidine kinase Hik33, which also partially controls the responses to osmotic, salt, and oxidative stress. This implies the existence of some universal, but yet unknown signal that triggers adaptive gene expression in response to various stressors. Here we selectively probed the components of photosynthetic machinery and functionally characterized the thermodynamics of cyanobacterial photosynthetic membranes with genetically altered fluidity. We show that the rate of oxidation of the quinone pool (PQ), which interacts with both photosynthetic and respiratory electron transport chains, depends on membrane fluidity. Inhibitor-induced stimulation of redox changes in PQ triggers cold-induced gene expression. Thus, the fluidity-dependent changes in the redox state of PQ may universally trigger cellular responses to stressors that affect membrane properties.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ETC:
-
Electron transport chain
- DCMU:
-
(3-(3,4-dichlorophenyl)-1,1-dimethylurea)
- DBMIB:
-
Dibromothymoquinone
- FA:
-
Fatty acid
- FAD:
-
Fatty acid desaturase
- FI:
-
Fluorescence induction
- MR:
-
Modulated reflection
- PQ:
-
Plastoquinone pool
- UFA:
-
Unsaturated fatty acid
References
Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681–1691. doi:10.1093/emboj/20.7.1681
Cooley JW, Vermaas WF (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J Bacteriol 183:4251–4258. doi:10.1128/JB.183.14.4251-4258.2001
Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550. doi:10.1104/pp.16.00375
Goldsmith RH, Moerner WE (2010) Watching conformational- and photodynamics of single fluorescent proteins in solution. Nat Chem 2:179–186. doi:10.1038/nchem.545
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2. A resolution role of quinones lipids channels and chloride. Nat Struct Mol Biol 16:334–342. doi:10.1038/nsmb.1559
He Q, Dolganov N, Bjorkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314. doi:10.1074/jbc.M008686200
Herbert SK, Martin RE, Fork DC (1995) Light adaptation of cyclic electron transport through Photosystem I in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 46:277–285. doi:10.1007/BF00020441
Kirilovsky D (2015) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126:3–17. doi:10.1007/s11120-014-0031-7
Kish E, Pinto MM, Kirilovsky D, Spezia R, Robert B (2015) Echinenone vibrational properties: from solvents to the orange carotenoid protein. Biochim Biophys Acta 1847:1044–1054. doi:10.1016/j.bbabio.2015.05.010
Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106. doi:10.1016/S0005-2728(98)00135-2
Koyama Y, Long RA, Martin WG, Carey PR (1979) The resonance Raman spectrum of carotenoids as an intrinsic probe for membrane potential. Oscillatory changes in the spectrum of neurosporene in the chromatophores of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 548:153–160. doi:10.1016/0005-2728(79)90196-8
Los DA, Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394:3–15. doi:10.1016/S0005-2760(98)00091-5
Los DA, Mironov KS, Allakhverdiev SI (2013) Regulatory role of membrane fluidity in gene expression and physiological functions. Photosynth Res 116:489–509. doi:10.1007/s11120-013-9823-4
Lutz M (1977) Antenna chlorophyll in photosynthetic membranes. A study by resonance Raman spectroscopy. Biochim Biophys Acta 460:408–430. doi:10.1016/0005-2728(77)90081-0
Maksimov EG, Kuzminov FI, Konyuhov IV, Elanskaya IV, Paschenko VZ (2011) Photosystem 2 effective fluorescence cross-section of cyanobacterium Synechocystis sp. PCC6803 and its mutants. J Photochem Photobiol B Biol 104:285–291. doi:10.1016/j.jphotobiol.2011.02.011
Maksimov EG, Shirshin EA, Sluchanko NN, Zlenko DV, Parshina EV, Tsoraev GV, Klementiev KE, Budylin GS, Schmitt F-J, Friedrich T, Fadeev VV, Paschenko VZ, Rubin AB (2015) The signaling state of orange carotenoid protein. Biophys J 109:595–607. doi:10.1016/j.bpj.2015.06.052
Mao H-B, Li G-F, Ruan X, Wu Q-Y, Gong Y-D, Zhang X-F, Zhao N-M (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b 6 f complex in Synechocystis sp. PCC 6803. FEBS Lett 519:82–86. doi:10.1016/S0014-5793(02)02715-1
Merlin JC (1985) Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems. Pure App Chem 57:785–792. doi:10.1351/pac198557050785
Mironov KS, Maksimov EG, Maksimov GV, Los DA (2012a) Feedback between fluidity of membranes and transcription of the desB gene for the ω3-desaturase in the cyanobacterium Synechocystis. Mol Biol 46:134–141. doi:10.1134/S002689331201013X
Mironov KS, Sidorov RA, Trofimova MS, Bedbenov VS, Tsydendambaev VD, Allakhverdiev SI, Los DA (2012b) Light-dependent cold-induced fatty acid unsaturation, changes in membrane fluidity, and alterations in gene expression in Synechocystis. Biochim Biophys Acta 1817:1352–1359. doi:10.1016/j.bbabio.2011.12.011
Mironov KS, Sidorov RA, Kreslavski VD, Bedbenov VS, Tsydendambaev VD, Los DA (2014) Cold-induced gene expression and ω3 fatty acid unsaturation is controlled by red light in Synechocystis. J Photochem Photobiol B 137:84–88. doi:10.1016/j.jphotobiol.2014.03.001
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. doi:10.1016/j.tplants.2011.03.007
Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta 1817:194–208. doi:10.1016/j.bbabio.2011.04.008
Mullineaux CW (2014) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:7. doi:10.3389/fpls.2014.00007
Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393. doi:10.1093/jxb/eri064
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371. doi:10.1016/S0092-8674(02)00867-X
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. doi:10.1016/j.bbabio.2006.11.019
Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin SA (ed) A-Z of quantitative PCR. International University Line, La Jolla, pp 87–112
Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27. doi:10.1016/0076-6879(88)67004-2
Saita E, Albanesi D, de Mendoza D (2016) Sensing membrane thickness: lessons learned from cold stress. Biochim Biophys Acta 1861:837–846. doi:10.1016/j.bbalip.2016.01.003
Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837:835–848. doi:10.1016/j.bbabio.2014.02.005
Sinetova MA, Los DA (2016a) New insights in cyanobacterial cold stress responses: genes, sensors, and molecular triggers. Biochim Biophys Acta 1860:2391–2403. doi:10.1016/j.bbagen.2016.07.006
Sinetova MA, Los DA (2016b) Systemic analysis of transcriptomics of Synechocystis: common stress genes and their universal triggers. Mol BioSyst 12:3254–3258. doi:10.1039/C6MB00551A
Sinetova MA, Los DA (2016c) Lessons from cyanobacterial transcriptomics: Universal genes and triggers of stress responses. Mol Biol 50:606–614. doi:10.1134/S0026893316040117
Sluchanko NN, Klementiev KE, Shirshin EA, Tsoraev GV, Friedrich T, Maksimov EG (2017) The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP. Biochim Biophys Acta 1858:1–11. doi:10.1016/j.bbabio.2016.10.005
Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327–1334. doi:10.1093/emboj/19.6.1327
Szalontai B, Gombos Z, Csizmadia V, Bagyinka C, Lutz M (1994) Structure and interactions of phycocyanobilin chromophores in phycocyanin and allophycocyanin from an analysis of their resonance Raman spectra. BioChemistry 33:11823–11832. doi:10.1021/bi00205a019
Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K, Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416–6425
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi:10.1093/nar/gkm306
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034
Vigh L, Los DA, Horvath I, Murata N (1993) 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. Proc Natl Acad Sci USA 90:9090–9094
Wu H, Volponi JV, Oliver AE, Parikh AN, Simmons BA, Sing S (2011) In vivo lipidomics using single-cell Raman spectroscopy. Proc Natl Acad Sci USA 108:3809–3814. doi:10.1073/pnas.1009043108
Yan J, Kurisu G, Cramer WA (2006) Intraprotein transfer of the quinone analogue inhibitor 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone in the cytochrome b6f complex. Proc Natl Acad Sci USA 103:69–74. doi:10.1073/pnas.0504909102
Zorina AA, Mironov KS, Stepanchenko NS, Sinetova MA, Koroban NV, Zinchenko VV, Kupriyanova EV, Allakhverdiev SI, Los DA (2011) Regulation systems for stress responses in cyanobacteria. Russ J Plant Physiol 58:749–767. doi:10.1134/S1021443711050281
Acknowledgements
This work was supported by the grant from Russian Science Foundation (14-24-00020) to D.A.L. E.G.M. was supported by a grant from Russian Foundation for Basic Research (No. 15-04-01930a), Russian Ministry of Education and Science (project MK-5949.2015.4), and by RFBR and Moscow city Government according to the research project no. 15-34-70007 «mol_а_mos». P.V.F. was supported by a grant from Russian Foundation for Basic Research (No. 16-34-50175 mol_nr). S.I.A. was supported by Russian Science Foundation (Grant No. 14-14-00039).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Maksimov, E.G., Mironov, K.S., Trofimova, M.S. et al. Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria. Photosynth Res 133, 215–223 (2017). https://doi.org/10.1007/s11120-017-0337-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0337-3