A Comprehensive Study of Light Quality Acclimation in Synechocystis Sp. PCC 6803

. 2024 Sep 03 ; 65 (8) : 1285-1297.

Jazyk angličtina Země Japonsko Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38907526

Grantová podpora
CZ.02.1.01/0.0/0.0/16_026/0008413 LM2018123 LUAUS24131 Ministerstvo Školství, Mládeže a Telovýchovy
K 140351 RRF-2.3.1-21-2022-00014 Nemzeti Kutatási, Fejlesztési és Innovaciós Alap
CZ.02.1.01/0.0/0.0/16_026/0008413 LM2018123 LUAUS24131 Ministerstvo Školství, Mládeže a Telovýchovy
K 140351 RRF-2.3.1-21-2022-00014 Nemzeti Kutatási, Fejlesztési és Innovaciós Alap

Cyanobacteria play a key role in primary production in both oceans and fresh waters and hold great potential for sustainable production of a large number of commodities. During their life, cyanobacteria cells need to acclimate to a multitude of challenges, including shifts in intensity and quality of incident light. Despite our increasing understanding of metabolic regulation under various light regimes, detailed insight into fitness advantages and limitations under shifting light quality remains underexplored. Here, we study photo-physiological acclimation in the cyanobacterium Synechocystis sp. PCC 6803 throughout the photosynthetically active radiation (PAR) range. Using light emitting diodes (LEDs) with qualitatively different narrow spectra, we describe wavelength dependence of light capture, electron transport and energy transduction to main cellular pools. In addition, we describe processes that fine-tune light capture, such as state transitions, or the efficiency of energy transfer from phycobilisomes to photosystems (PS). We show that growth was the most limited under blue light due to inefficient light harvesting, and that many cellular processes are tightly linked to the redox state of the plastoquinone (PQ) pool, which was the most reduced under red light. The PSI-to-PSII ratio was low under blue photons, however, it was not the main growth-limiting factor, since it was even more reduced under violet and near far-red lights, where Synechocystis grew faster compared to blue light. Our results provide insight into the spectral dependence of phototrophic growth and can provide the foundation for future studies of molecular mechanisms underlying light acclimation in cyanobacteria, leading to light optimization in controlled cultivations.

Zobrazit více v PubMed

Ajlani  G. and Vernotte  C. (1998) Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol. Biol.  37: 577–580. PubMed

Bečková  M., Sobotka  R. and Komenda  J. (2022) Photosystem II antenna modules CP43 and CP47 do not form a stable ‘no reaction centre complex’ in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth. Res.  152: 363–371. PubMed PMC

Bernát  G., Steinbach  G., Kaňa  R., Govindjee, Misra  A.N., Prašil  O. and Prašil  O. (2018) On the origin of the slow M–T chlorophyll a fluorescence decline in cyanobacteria: interplay of short-term light-responses. Photosynth. Res.  136: 183–198. PubMed

Bernát  G., Zavřel  T., Kotabová  E., Kovács  L., Steinbach  G., Vörös  L., et al. (2021) Photomorphogenesis in the picocyanobacterium Cyanobium gracile includes increased phycobilisome abundance under blue light, phycobilisome decoupling under near far-red light, and wavelength-specific photoprotective strategies. Front Plant Sci.  12: 1–16. PubMed PMC

Calzadilla  P.I. and Kirilovsky  D. (2020) Revisiting cyanobacterial state transitions. Photochem. Photobiol. Sci.  19: 585–603. PubMed

Cano  M., Holland  S.C., Artier  J., Burnap  R.L., Ghirardi  M., Morgan  J.A., et al. (2018) Glycogen synthesis and metabolite overflow contribute to energy balancing in cyanobacteria. Cell Rep.  23: 667–672. PubMed

de Mendiburu  F. and Yaseen  M. (2020) Agricolae: statistical procedures for agricultural research.

Demmig‐Adams  B. and Adams  W.W. (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol.  172: 11–21. PubMed

Felcmanová  K., Lukeš  M., Kotabová  E., Lawrenz  E., Halsey  K.H. and Prášil  O. (2017) Carbon use efficiencies and allocation strategies in Prochlorococcus marinus strain PCC 9511 during nitrogen-limited growth. Photosynth. Res.  134: 71–82. PubMed

Fox  J. and Weisberg  S. (2019) An R Companion to Applied Regression, Third. Sage, Thousand Oaks CA.

Foyer  C.H., Neukermans  J., Queval  G., Noctor  G. and Harbinson  J. (2012) Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot.  63: 1637–1661. PubMed

Giraudoux  P., Antonietti  J.-P., Beale  C., Groemping  U., Lancelot  R., Pleydell  D., et al. (2023) pgirmess: spatial analysis and data mining for field ecologists.

Grébert  T., Doré  H., Partensky  F., Farrant  G.K., Boss  E.S., Picheral  M., et al. (2018) Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria. Proc. Natl. Acad. Sci. U. S. A.  115: E2010–E2019. PubMed PMC

Hirose  Y., Chihong  S., Watanabe  M., Yonekawa  C., Murata  K., Ikeuchi  M., et al. (2019) Diverse chromatic acclimation processes regulating phycoerythrocyanin and rod-shaped phycobilisome in cyanobacteria. Mol. Plant  12: 715–725. PubMed

Holtrop  T., Huisman  J., Stomp  M., Biersteker  L., Aerts  J., Grébert  T., et al. (2021) Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans. Nat. Ecol. Evol.  5: 55–66. PubMed

Hübschmann  T., Yamamoto  H., Gieler  T., Murata  N. and Börner  T. (2005) Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: impact of cyanobacterial phytochromes. Febs. Lett.  579: 1613–1618. PubMed

Jahn  M., Vialas  V., Karlsen  J., Ka  L., Uhle  M. and Hudson  E.P. (2018) Growth of cyanobacteria is constrained by the abundance of light and carbon assimilation proteins. Cell Rep.  25: 478–486. PubMed

Kirilovsky  D. and Kerfeld  C.A. (2016) Cyanobacterial photoprotection by the orange carotenoid protein. Nat. Plants  2: 1–7. PubMed

Klaus  O., Hilgers  F., Nakielski  A., Hasenklever  D., Jaeger  K.E., Axmann  I.M., et al. (2022) Engineering phototrophic bacteria for the production of terpenoids. Curr. Opin. Biotechnol.  77: 1–10. PubMed

Kondo  K., Mullineaux  C.W. and Ikeuchi  M. (2009) Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803. Photosynth. Res.  99: 217–225. PubMed

Krieger-Liszkay  A. (2004) Singlet oxygen production in photosynthesis. J. Exp. Bot.  56: 337–346. PubMed

Li  M., Ma  J., Li  X. and Sui  S.-F. (2021) In situ cryo-ET structure of phycobilisome–photosystem II supercomplex from red alga. Elife  10: 1–19. PubMed PMC

Luimstra  V.M., Schuurmans  J.M., Hellingwerf  K.J., Matthijs  H.C.P. and 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. PubMed PMC

Luimstra  V.M., Schuurmans  J.M., Verschoor  A.M., Hellingwerf  K.J., Huisman  J. and Matthijs  H.C.P. (2018) Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II. Photosynth. Res.  138: 177–189. PubMed PMC

Montgomery  B.L. (2016) Mechanisms and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria. J. Exp. Bot.  67: 4079–4090. PubMed

Müller  S., Zavřel  T. and Červený  J. (2019) Towards a quantitative assessment of inorganic carbon cycling in photosynthetic microorganisms. Eng. Life Sci.  19: 955–967. PubMed PMC

Murakami  A., Kim  S.J. and 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. PubMed

Netzer-El  S.Y., Caspy  I. and Nelson  N. (2019) Crystal structure of photosystem I monomer from synechocystis PCC 6803. Front Plant Sci.  9: 1–7. PubMed PMC

Pfennig  T., Kullmann  E., Zavřel  T., Nakielski  A., Ebenhöh  O., Červený  J., et al. (2023) Shedding light on blue-green photosynthesis: a wavelength-dependent mathematical model of photosynthesis in synechocystis sp. PCC 6803. bioRxiv. 1–23.

Pospíšil  P. (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim. Biophys. Acta - Bioenergy  1817: 218–231. PubMed

R Core Team . (2022) R: A language and environment for statistical computing.

Remelli  W. and Santabarbara  S. (2018) Excitation and emission wavelength dependence of fluorescence spectra in whole cells of the cyanobacterium Synechocystis sp. PPC6803: influence on the estimation of Photosystem II maximal quantum efficiency. BBA - Bioenerg.  1859: 1207–1222. PubMed

Rippka  R., Deruelles  J., Waterbury  J.B., Herdman  M. and Stanier  R.Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology  111: 1–61.

Rodrigues  J.S., Kovács  L., Lukeš  M., Höper  R., Steuer  R., Červený  J., et al. (2023) Characterizing isoprene production in cyanobacteria – Insights into the effects of light, temperature, and isoprene on Synechocystis sp. PCC 6803. Bioresour. Technol.  380: 1–10. PubMed

Sanfilippo  J.E., Garczarek  L., Partensky  F. and Kehoe  D.M. (2019) Chromatic acclimation in cyanobacteria: a diverse and widespread process for optimizing photosynthesis. Annu. Rev. Microbiol.  73: 407–433. PubMed

Schreiber  U., Klughammer  C. and Kolbowski  J. (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth. Res.  113: 127–144. PubMed PMC

Singh  A.K., Bhattacharyya-Pakrasi  M., Elvitigala  T., Ghosh  B., Aurora  R. and Pakrasi  H.B. (2009) A systems-level analysis of the effects of light quality on the metabolism of a cyanobacterium. Plant Physiol.  151: 1596–1608. PubMed PMC

Singh  S.P., Der  D.H.Ã. and Sinha  R.P. (2010) Cyanobacteria and ultraviolet radiation (UVR) stress;: mitigation strategies. Ageing. Res. Rev.  9: 79–90. PubMed

Stirbet  A., Lazár  D., Kromdijk  J. and Govindjee  G. (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses?  Photosynthetica  56: 86–104.

Tamary  E., Kiss  V., Nevo  R., Adam  Z., Bernát  G., Rexroth  S., et al. (2012) Structural and functional alterations of cyanobacterial phycobilisomes induced by high-light stress. Biochim. Biophys. Acta - Bioenergy  1817: 319–327. PubMed

Tchernov  D., Silverman  J., Luz  B., Reinhold  L. and Kaplan  A. (2003) Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. Photosynth. Res.  77: 95–103. PubMed

Tóth  S.Z., Schansker  G. and Strasser  R.J. (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth. Res.  93: 193–203. PubMed

Tsimilli-Michael  M., Stamatakis  K. and Papageorgiou  G.C. (2009) Dark-to-light transition in Synechococcus sp. PCC 7942 cells studied by fluorescence kinetics assesses plastoquinone redox poise in the dark and photosystem II fluorescence component and dynamics during state 2 to state 1 transition. Photosynth. Res.  99: 243–255. PubMed

Tsuyama  M., Shibata  M., Kawazu  T. and Kobayashi  Y. (2004) An analysis of the mechanism of the low-wave phenomenon of chlorophyll fluorescence. Photosynth. Res.  81: 67–76. PubMed

Umena  Y., Kawakami  K., Shen  J.-R. and Kamiya  N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature  473: 55–60. PubMed

Wang  F. and Chen  M. (2022) Chromatic acclimation processes and their relationships with phycobiliprotein complexes. Microorganisms  10: 2–15. PubMed PMC

Wilde  A., Churin  Y., Schubert  H. and Börner  T. (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. Febs. Lett.  406: 89–92. PubMed

Wiltbank  L.B. and Kehoe  D.M. (2019) Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nat Rev Microbiol.  17: 37–50. PubMed

Zakar  T., Herman  E., Vajravel  S., Kovacs  L., Knoppová  J., Komenda  J., et al. (2017) Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis sp. PCC6803. Biochim. Biophys. Acta - Bioenergy  1858: 337–350. PubMed PMC

Zavřel  T., Chmelík  D., Sinetova  M.A. and Červený  J. (2018a) Spectrophotometric determination of phycobiliprotein content in cyanobacterium synechocystis. J. Vis. Exp.  139  1–9. PubMed PMC

Zavřel  T., Faizi  M., Loureiro  C., Sinetova  M., Zorina  A., Poschmann  G., et al. (2019) Quantitative insights into the cyanobacterial cell economy. Elife  8: 1–29. PubMed PMC

Zavřel  T., Očenášová  P., Červený  J. and Jacobs  J.M. (2017) Phenotypic characterization of Synechocystis sp. PCC 6803 substrains reveals differences in sensitivity to abiotic stress. PLoS One  12: 1–21. PubMed PMC

Zavřel  T., Očenášová  P., Sinetova  M. and Červený  J. (2018b) Determination of storage (starch/glycogen) and total saccharides content in algae and cyanobacteria by a phenol-sulfuric acid method. Bio-Protocol  8: 1–13. PubMed PMC

Zavřel  T., Schoffman  H., Lukeš  M., Fedorko  J., Keren  N. and Červený  J. (2021) Monitoring fitness and productivity in cyanobacteria batch cultures. Algal. Res.  56: 1–15.

Zavřel  T., Sinetova  M.A., Búzová  D., Literáková  P. and Červený  J. (2015a) Characterization of a model cyanobacterium Synechocystis sp. PCC 6803 autotrophic growth in a flat-panel photobioreactor. Eng. Life Sci.  15: 122–132.

Zavřel  T., Sinetova  M.A. and Červený  J. (2015b) Measurement of chlorophyll a and carotenoids concentration in Cyanobacteria. bio-protocol  5: 1–5.

Zavřel  T., Szabó  M., Tamburic  B., Evenhuis  C., Kuzhiumparambil  U., Literáková  P., et al. (2018c) Effect of carbon limitation on photosynthetic electron transport in Nannochloropsis oculata. J. Photochem. Photobiol. B: Biol.  181: 31–43. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...