Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
33304364
PubMed Central
PMC7693714
DOI
10.3389/fpls.2020.586543
Knihovny.cz E-resources
- Keywords
- cyanobacteria, membrane organization, microdomains and rafts, phenotypic heterogeneity, photosynthesis, photosystems, phycobilisomes decoupling, thylakoid membrane,
- Publication type
- Journal Article MeSH
Photosynthetic light reactions proceed in thylakoid membranes (TMs) due to the activity of pigment-protein complexes. These complexes are heterogeneously organized into granal/stromal thylakoids (in plants) or into recently identified cyanobacterial microdomains (MDs). MDs are characterized by specific ratios of photosystem I (PSI), photosystem II (PSII), and phycobilisomes (PBS) and they are visible as sub-micrometer sized areas with different fluorescence ratios. In this report, the process of long-term plasticity in cyanobacterial thylakoid MDs has been explored under variable growth light conditions using Synechocystis sp. PCC6803 expressing YFP tagged PSI. TM organization into MDs has been observed for all categorized shapes of cells independently of their stage in cell cycle. The heterogeneous PSI, PSII, and PBS thylakoid areas were also identified under two types of growth conditions: at continuous light (CL) and at light-dark (L-D) cycle. The acclimation from CL to L-D cycle changed spatial distribution of photosystems, in particular PSI became more evenly distributed in thylakoids under L-D cycle. The process of the spatial PSI (and partially also PSII) redistribution required 1 week and was accompanied by temporal appearance of PBS decoupling probably caused by the re-organization of photosystems. The overall acclimation we observed was defined as TM plasticity as it resembles higher plants grana/stroma reorganization at variable growth light conditions. In addition, we observed large cell to cell variability in the actual MDs organization. It leads us to suggest that the plasticity, and cell to cell variability in MDs could be a manifestation of phenotypic heterogeneity, a recently broadly discussed phenomenon for prokaryotes.
Faculty of Science University of South Bohemia České Budějovice Czechia
Institute of Microbiology CAS Centrum Algatech Třeboň Czechia
See more in PubMed
Ackermann M. (2015). A functional perspective on phenotypic heterogeneity in microorganisms. Nat. Rev. Microbiol. 13 497–508. 10.1038/nrmicro3491 PubMed DOI
Albertsson P. -Å. (2001). A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6 349–354. 10.1016/s1360-1385(01)02021-0 PubMed DOI
Andersson B., Anderson J. M. (1980). Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach-chloroplasts. Biochim. Biophys. Acta 593 427–440. 10.1016/0005-2728(80)90078-x PubMed DOI
Bald D., Kruip J., Rogner M. (1996). Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth. Res. 49 103–118. 10.1007/bf00117661 PubMed DOI
Baulina O. I. (2012). “Ultrastructural plasticity of cyanobacteria under dark and high light intensity conditions,” in Ultrastructural Plasticity of Cyanobacteria, (Berlin: Springer-Verlag; ), 11–63. 10.1007/978-3-642-32781-0_2 DOI
Bišová K., Zachleder V. (2014). Cell-cycle regulation in green algae dividing by multiple fission. J. Exp. Bot. 65 2585–2602. 10.1093/jxb/ert466 PubMed DOI
Calzadilla P. I., Kirilovsky D. (2020). Revisiting cyanobacterial state transitions. Photochem. Photobiol. Sci. 19 585–603. 10.1039/c9pp00451c PubMed DOI
Casella S., Huang F., Mason D., Zhao G. Y., Johnson G. N., Mullineaux C. W., et al. (2017). Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol. Plant 10 1434–1448. 10.1016/j.molp.2017.09.019 PubMed DOI PMC
Chukhutsina V., Bersanini L., Aro E.-M., van Amerongen H. (2015). Cyanobacterial light-harvesting phycobilisomes uncouple from photosystem i during dark-to-light transitions. Sci. Rep. 5:14193. PubMed PMC
Collins A. M., Liberton M., Jones H. D. T., Garcia O. F., Pakrasi H. B., Timlin J. A. (2012). Photosynthetic pigment localization and thylakoid membrane morphology are altered in synechocystis 6803 phycobilisome mutants. Plant Physiol. 158 1600–1609. 10.1104/pp.111.192849 PubMed DOI PMC
de Mendiburu F. (2020). agricolae: Statistical Procedures for Agricultural Research. 10.1104/pp.111.192849. Available online at: https://cran.r-project.org/web/packages/agricolae/index.html PubMed DOI PMC
Diamond S., Jun D. R., Rubin B. E., Golden S. S. (2015). The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth. Proc. Natl. Acad. Sci. U.S.A. 112 E1916–E1925. PubMed PMC
Duncan D. B. (1955). Multiple range and multiple F tests. Biometrics 11 1–42. 10.2307/3001478 DOI
El Bissati K., Kirilovsky D. (2001). Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol. 125 1988–2000. 10.1104/pp.125.4.1988 PubMed DOI PMC
Fisher R. A. (1921). On the “Probable Error” of a coefficient of correlation deduced from a small sample. Metron 1 3–32.
Flores E., Herrero A. (2005). Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem. Soc. Trans. 33 164–167. 10.1042/bst0330164 PubMed DOI
Grote J., Krysciak D., Streit W. R. (2015). Phenotypic heterogeneity, a phenomenon that may explain why quorum sensing does not always result in truly homogenous cell behavior. Appl. Environ. Microbiol. 81 5280–5289. 10.1128/aem.00900-15 PubMed DOI PMC
Herbstova M., Tietz S., Kinzel C., Turkina M. V., Kirchhoff H. (2012). Architectural switch in plant photosynthetic membranes induced by light stress. Proc. Natl. Acad. Sci. U.S.A. 109 20130–20135. 10.1073/pnas.1214265109 PubMed DOI PMC
Kaňa R. (2013). Mobility of photosynthetic proteins. Photosynth. Res. 116 465–479. 10.1007/s11120-013-9898-y PubMed DOI
Kaňa R., Govindjee (2016). Role of ions in the regulation of light-harvesting. Front. Plant Sci. 7:1849. 10.3389/fpls.2016.01849 PubMed DOI PMC
Kaňa R., Kotabová E., Komárek O., Šedivá B., Papageorgiou G. C., Govindjee, et al. (2012). The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim. Biophys. Acta Bioenerg. 1817 1237–1247. 10.1016/j.bbabio.2012.02.024 PubMed DOI
Kaňa R., Prášil O., Komárek O., Papageorgiou G. C., Govindjee (2009). Spectral characteristic of fluorescence induction in a model cyanobacterium, Synechococcus sp (PCC 7942). Biochim. Biophys. Acta 1787 1170–1178. 10.1016/j.bbabio.2009.04.013 PubMed DOI
Kirchhoff H. (2008). Significance of protein crowding, order and mobility for photosynthetic membrane functions. Biochem. Soc. Trans. 36 967–970. 10.1042/bst0360967 PubMed DOI
Kirchhoff H. (2013). Architectural switches in plant thylakoid membranes. Photosynth. Res. 116 481–487. 10.1007/s11120-013-9843-0 PubMed DOI
Kirilovsky D., Kaňa R., Prášil O. (2014). “Mechanisms modulating energy arriving at reaction centers in cyanobacteria,” in Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria, Vol. 40 eds Demmig-Adams B., Garab G., Iii W. A., Govindjee (Dordrecht: Springer Netherlands; ), 471–501. 10.1007/978-94-017-9032-1_22 DOI
Konert G., Steinbach G., Canonico M., Kaňa R. (2019). Protein arrangement factor: a new photosynthetic parameter characterizing the organization of thylakoid membrane proteins. Physiol. Plant. 166 264–277. 10.1111/ppl.12952 PubMed DOI
Kopečná J., Komenda J., Bučinská L., Sobotka R. (2012). Long-term acclimation of the cyanobacterium Synechocystis PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric PSI. Plant Physiol. 160 2239–2250. 10.1104/pp.112.207274 PubMed DOI PMC
Kupper H., Andresen E., Wiegert S., Simek M., Leitenmaier B., Šetlik I. (2009). Reversible coupling of individual phycobiliprotein isoforms during state transitions in the cyanobacterium Trichodesmium analysed by single-cell fluorescence kinetic measurements. Biochim. Biophys. Acta 1787 155–167. 10.1016/j.bbabio.2009.01.001 PubMed DOI
Li L., Aro E. M., Millar A. H. (2018). Mechanisms of photodamage and protein turnover in photoinhibition. Trends Plant Sci. 23 667–676. 10.1016/j.tplants.2018.05.004 PubMed DOI
Li Z. R., Wakao S., Fischer B. B., Niyogi K. K. (2009). Sensing and responding to excess light. Annu. Rev. Plant Biol. 60 239–260. 10.1146/annurev.arplant.58.032806.103844 PubMed DOI
Luimstra V. M., Schuurmans J. M., Hellingwerf K. J., Matthijs H. C. P., Huisman J. (2020). Blue light induces major changes in the gene expression profile of the cyanobacterium Synechocystis sp. PCC 6803. Physiol. Plant. 170 10–26. 10.1111/ppl.13086 PubMed DOI PMC
Martins B. M. C., Tooke A. K., Thomas P., Locke J. C. W. (2018). Cell size control driven by the circadian clock and environment in cyanobacteria. Proc. Natl. Acad. Sci. U.S.A. 115 E11406–E11424. 10.1002/(sici)1521-1878(200001)22:1¡10::aid-bies4¿3.0.co;2-a PubMed DOI PMC
McConnell M. D., Koop R., Vasil’ev S., Bruce D. (2002). Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol. 130 1201–1212. 10.1104/pp.009845 PubMed DOI PMC
Mullineaux C. W. (2005). Function and evolution of grana. Trends Plant Sci. 10 521–525. 10.1016/j.tplants.2005.09.001 PubMed DOI
Mullineaux C. W. (2008). Factors controlling the mobility of photosynthetic proteins. Photochem. Photobiol. 84 1310–1316. 10.1111/j.1751-1097.2008.00420.x PubMed DOI
Murakami A., Fujita Y. (1993). regulation of stoichiometry between PSI and PSII in response to light regime for photosynthesis observed with synechocystis PCC-6714 – relationship between redox state of CYT B6-F complex and regulation of PSI formation. Plant Cell Physiol. 34 1175–1180.
Murakami A., Kim S. J., Fujita Y. (1997). Changes in photosystem stoichiometry in response to environmental conditions for cell growth observed with the cyanophyte Synechocystis PCC 6714. Plant Cell Physiol. 38 392–397. 10.1093/oxfordjournals.pcp.a029181 PubMed DOI
Murakami S., Packer L. (1970). Light-induced changes in conformation and configuration of thylakoid membrane of ulva and porphyra chloroplasts in-vivo. Plant Physiol. 45 289–299. 10.1104/pp.45.3.289 PubMed DOI PMC
Nagy G., Posselt D., Kovács L., Holm J. K., Szabó M., Ughy B., et al. (2011). Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering. Biochem. J. 436 225–230. 10.1042/bj20110180 PubMed DOI
Nedbal L., Trtílek M., Cervený J., Komárek O., Pakrasi H. B. (2008). A photobioreactor system for precision cultivation of photoautotrophic microorganisms and for high-content analysis of suspension dynamics. Biotechnol. Bioeng. 100 902–910. 10.1002/bit.21833 PubMed DOI
Nishihama R., Kohchi T. (2013). Evolutionary insights into photoregulation of the cell cycle in the green lineage. Curr. Opin. Plant Biol. 16 630–637. 10.1016/j.pbi.2013.07.006 PubMed DOI
Nordholt N., van Heerden J. H., Bruggeman F. J. (2020). Biphasic cell-size and growth-rate homeostasis by single Bacillus subtilis cells. Curr. Biol. 30 2238–2247.e5. PubMed
Olive J., Ajlani G., Astier C., Recouvreur M. (1997). Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803. Biochim. Biophys. Acta 1319 275–282. 10.1016/s0005-2728(96)00168-5 DOI
Olive J., Mbina I., Vernotte C., Astier C., Wollman F. A. (1986). Randomization of the ef particles in thylakoid membranes of synechocystis-6714 upon transition from state-i to state-ii. FEBS Lett. 208 308–312. 10.1016/0014-5793(86)81039-0 DOI
Pribil M., Labs M., Leister D. (2014). Structure and dynamics of thylakoids in land plants. J. Exp. Bot. 65 1955–1972. 10.1093/jxb/eru090 PubMed DOI
Ranjbar Choubeh R., Wientjes E., Struik P. C., Kirilovsky D., van Amerongen H. (2018). State transitions in the cyanobacterium Synechococcus elongatus 7942 involve reversible quenching of the photosystem II core. Biochim. Biophys. Acta Bioenerg. 1859 1059–1066. 10.1016/j.bbabio.2018.06.008 PubMed DOI
RCoreTeam (2019). R: A Language and Environment for Statistical Computing. Available online at: http://www.r-project.org/index.html
RStudioTeam (2019). RStudio: Integrated Development Environment for R. Available online at: http://www.rstudio.com/
Sarcina M., Bouzovitis N., Mullineaux C. W. (2006). Mobilization of photosystem II induced by intense red light in the cyanobacterium Synechococcus sp PCC7942. Plant Cell 18 457–464. 10.1105/tpc.105.035808 PubMed DOI PMC
Schneider D., Fuhrmann E., Scholz I., Hess W. R., Graumann P. L. (2007). Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol. 8:10. 10.1186/1471-2121-8-39 PubMed DOI PMC
Signorell et mult. al A. (2020). DescTools: Tools for Descriptive Statistics. Available online at: https://cran.r-project.org/package=DescTools
Steinbach G., Kaňa R. (2016). Automated microscopy: macro language controlling a confocal microscope and its external illumination: adaptation for photosynthetic organisms. Microsc. Microanal. 22 258–263. 10.1017/s1431927616000556 PubMed DOI
Stingaciu L.-R., O’Neill H. M., Liberton M., Pakrasi H. B., Urban V. S. (2019). Influence of chemically disrupted photosynthesis on cyanobacterial thylakoid dynamics in Synechocystis sp. PCC 6803. Sci. Rep. 9: 5711. PubMed PMC
Strašková A., Knoppová J., Komenda J. (2018). Isolation of the cyanobacterial YFP-tagged photosystem I using GFP-Trap (R). Photosynthetica 56 300–305. 10.1007/s11099-018-0771-2 DOI
Strašková A., Steinbach G., Konert G., Kotabová E., Komenda J., Tichı M., et al. (2019). Pigment-protein complexes are organized into stable microdomains in cyanobacterial thylakoids. Biochim. Biophys. Acta Bioenerg. 1860:148053. 10.1016/j.bbabio.2019.07.008 PubMed DOI
Student. (1908). The probable error of a mean. Biometrika 6 1–25. 10.2307/2331554 DOI
Tamary E., Kiss V., Nevo R., Adam Z., Bernat G., Rexroth S., et al. (2012). Structural and functional alterations of cyanobacterial phycobilisomes induced by high-light stress. Biochim. Biophys. Acta Bioenerg. 1817 319–327. 10.1016/j.bbabio.2011.11.008 PubMed DOI
van Alphen P., Hellingwerf K. J. (2015). Sustained circadian rhythms in continuous light in Synechocystis sp. PCC6803 growing in a well-controlled photobioreactor. PLoS One 10:e0127715. 10.1371/journal.pone.0127715 PubMed DOI PMC
Van Boxtel C., Van Heerden J. H., Nordholt N., Schmidt P., Bruggeman F. J. (2017). Taking chances and making mistakes: non-genetic phenotypic heterogeneity and its consequences for surviving in dynamic environments. J. R. Soc. Interface 14:20170141. 10.1098/rsif.2017.0141 PubMed DOI PMC
Welkie D. G., Rubin B. E., Diamond S., Hood R. D., Savage D. F., Golden S. S. (2019). A hard day’s night: cyanobacteria in diel cycles. Trends Microbiol. 27 231–242. 10.1016/j.tim.2018.11.002 PubMed DOI PMC
Wickham H., François R., Lionel H., Müller K. (2020). dplyr: A Grammar of Data Manipulation. Available online at: https://dplyr.tidyverse.org/
Yang Q., Pando B. F., Dong G., Golden S. S., van Oudenaarden A. (2010). Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 327 1522–1526. 10.1126/science.1181759 PubMed DOI PMC
Yu F. B., Willis L., Chau R. M. W., Zambon A., Horowitz M., Bhaya D., et al. (2017). Long-term microfluidic tracking of coccoid cyanobacterial cells reveals robust control of division timing. BMC Biol. 15:11. 10.1186/s12915-016-0344-4 PubMed DOI PMC
Fast Diffusion of the Unassembled PetC1-GFP Protein in the Cyanobacterial Thylakoid Membrane