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Photosynthetica

, Volume 56, Issue 1, pp 192–199 | Cite as

Regulating photoprotection improves photosynthetic growth and biomass production in QC-site mutant cells of the cyanobacterium Synechocystis sp. PCC 6803

  • J.-Y. Huang
  • N.-T. Hung
  • K.-M. Lin
  • Y.-F. Chiu
  • H.-A. Chu
Article

Abstract

We characterized the photosynthetic growth of wild-type (WT) and QC-site mutant cells of the cyanobacterium Synechocystis sp. PCC 6803 grown in a photobioreactor under medium-intensity [~70 μmol(photon) m–2 s–1] and high-intensity [~200 μmol(photon) m–2 s–1] light conditions. Photosynthetic growth rate (the exponential phase) increased about 1.1–1.2 fold for the A16FJ, S28Aβ, and V32Fβ mutant compared with WT cells under medium-intensity light and about 1.2–1.3 fold under high-intensity light. Biomass production increased about 17–20% for A16FJ and S28Aβ mutant cells as compared with WT cells under medium-intensity light and about 14–17% for A16FJ and V32Fβ mutant cells under high-intensity light. The greater photosynthetic growth rate and biomass production of these QC-site mutant cells could be attributed to the increased photosynthesis efficiency and decreased dissipation of wasteful energy from phycobilisomes in mutants vs. WT cells. Our results support that manipulation of photoprotection may improve photosynthesis and biomass production of photosynthetic organisms.

Additional key words

cytochrome b559 photosynthesis photosystem II photoprotection QC 

Abbreviations

Chl

chlorophyll

Cyt

cytochrome

Fm

the maximal fluorescence yield

Fm,dark

the maximal fluorescence yield in the dark

F0

the dark fluorescence yield

HP

high- potential form

IP

intermedium potential form

LP

low-potential form

NPQ

nonphotochemical fluorescence quenching

OCP

orange carotenoid proteins

PQ

plastoquinone

WT

wild-type control Synechocystis strain constructed in the same manner as site-directed mutants but with no mutation

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References

  1. Al-Haj L., Lui Y.T., Abed R.M. et al.: Cyanobacteria as chassis for industrial biotechnology: progress and prospects.–Life (Basel) 6: E42, 2016.Google Scholar
  2. Bondarava N., De Pascalis L., Al-Babili S. et al.: Evidence that cytochrome b559 mediates the oxidation of reduced plasto quinone in the dark.–J. Biol. Chem. 278: 13554–13560, 2003.CrossRefPubMedGoogle Scholar
  3. Bondarava N., Gross C.M., Mubarakshina M. et al.: Putative function of cytochrome b559 as a plastoquinol oxidase.–Physiol. Plantarum 138: 463–473, 2010.CrossRefGoogle Scholar
  4. Boulay C., Wilson A., D’Haene S. et al.: Identification of a protein required for recovery of full antenna capacity in OCPrelated photoprotective mechanism in cyanobacteria.–P. Natl. Acad. Sci. USA 107: 11620–11625, 2010.CrossRefGoogle Scholar
  5. Bruce D., Brimble S., Bryant D.A.: State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002.–Biochim. Biophys. Acta 974: 66–73, 1989.CrossRefPubMedGoogle Scholar
  6. Chiu Y.F., Chen Y.H., Roncel M. et al.: Spectroscopic and functional characterization of cyanobacterium Synechocystis PCC 6803 mutants on the cytoplasmic-side of cytochrome b559 in photosystem II.–Biochim. Biophys. Acta 1827: 507–519, 2013.CrossRefPubMedGoogle Scholar
  7. Chiu Y.F., Lin W.C., Wu C.M. et al.: Identification and characterization of a cytochrome b559 Synechocystis 6803 mutant spontaneously generated from DCMU-inhibited photoheterotrophical growth conditions.–Biochim. Biophys. Acta 1787: 1179–1188, 2009.CrossRefPubMedGoogle Scholar
  8. Chu H.A., Chiu Y.F.: The roles of cytochrome b559 in assembly and photoprotection of photosystem II revealed by site-directed mutagenesis studies.–Front. Plant Sci. 6: 1261, 2015.CrossRefPubMedGoogle Scholar
  9. Gao X., Sun T., Pei G. et al.: Cyanobacterial chassis engineering for enhancing production of biofuels and chemicals.–Appl. Microbiol. Biotechnol. 100: 3401–3413, 2016.CrossRefPubMedGoogle Scholar
  10. Guskov A., Kern J., Gabdulkhakov A. et al.: Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride.–Nat. Struct. Mol. Biol. 16: 334–342, 2009.CrossRefPubMedGoogle Scholar
  11. Hasegawa K., Noguchi T.: Molecular interactions of the quinone electron acceptors QA, QB, and QC in photosystem II as studied by the fragment molecular orbital method.–Photosynth. Res. 120: 113–123, 2014.CrossRefPubMedGoogle Scholar
  12. Huang J.Y., Chiu Y.F., Ortega J.M. et al.: Mutations of cytochrome b559 and psbJ on and near the QC Site in photosystem II influence the regulation of short-term light response and photosynthetic growth of the cyanobacterium Synechocystis sp. PCC 6803.–Biochemistry 55: 2214–2226, 2016.CrossRefPubMedGoogle Scholar
  13. Hung C.H., Huang J.Y., Chiu Y.F. et al.: Site-directed mutagenesis on the heme axial-ligands of cytochrome b559 in photosystem II by using cyanobacteria Synechocystis PCC 6803.–Biochim. Biophys. Acta 1767: 686–693, 2007.CrossRefPubMedGoogle Scholar
  14. Hung C.H., Hwang H.J., Chen Y.H. et al.: Spectroscopic and functional characterizations of cyanobacterium Synechocystis PCC 6803 mutants on and near the heme axial ligand of cytochrome b559 in photosystem II.–J. Biol. Chem. 285: 5653–5663, 2010.CrossRefPubMedGoogle Scholar
  15. Kaminskaya O., Shuvalov V.A., Renger G.: Evidence for a novel quinone-binding site in the photosystem II (PS II) complex that regulates the redox potential of cytochrome b559.–Biochemistry 46: 1091–1105, 200CrossRefPubMedGoogle Scholar
  16. Kaminskaya O., Shuvalov V.A., Renger G.: Two reaction pathways for transformation of high potential cytochrome b559 of PS II into the intermediate potential form.–BBA-Bioenergetics 1767: 550–558, 2007b.CrossRefPubMedGoogle Scholar
  17. Kaminskaya O.P., Shuvalov V.A.: Biphasic reduction of cytochrome b559 by plastoquinol in photosystem II membrane fragments: evidence for two types of cytochrome b559/ plastoquinone redox equilibria.–BBA-Bioenergetics 1827: 471–483, 2013.CrossRefPubMedGoogle Scholar
  18. Kirilovsky D.: Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions.–Photosynth. Res. 126: 3–17, 2015.CrossRefPubMedGoogle Scholar
  19. Kirilovsky D., Kerfeld C.A.: Cyanobacterial photoprotection by the orange carotenoid protein.–Nat. Plants 2: 16180, 2016. doi: 10.1038/nplants.2016.180CrossRefPubMedGoogle Scholar
  20. Komenda J., Reisinger V., Müller B.C. et al.: Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803.–J. Biol. Chem. 279: 48620–48629, 2004.CrossRefPubMedGoogle Scholar
  21. Kondo K., Mullineaux C.W., Ikeuchi M.: Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803.–Photosynth. Res. 99: 217–225, 2009.CrossRefPubMedGoogle Scholar
  22. Kromdijk J., Głowacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection.–Science 354: 857–861, 2016.CrossRefPubMedGoogle Scholar
  23. Kruk J., Strzałka K.: Redox changes of cytochrome b559 in the presence of plastoquinones.–J. Biol. Chem. 276: 86–91, 2001.CrossRefPubMedGoogle Scholar
  24. Kruk J., Strzałka K.: Dark reoxidation of the plastoquinone-pool is mediated by the low-potential form of cytochrome b559 in spinach thylakoids.–Photosynth. Res. 62: 273–279, 1999.CrossRefGoogle Scholar
  25. Machado I.M., Atsumi S.: Cyanobacterial biofuel production.–J. Biotechnol. 162: 50–56, 2012.CrossRefPubMedGoogle Scholar
  26. Morais F., Barber J., Nixon P.J.: The chloroplast-encoded alpha subunit of cytochrome b559 is required for assembly of the photosystem two complex in both the light and the dark in Chlamydomonas reinhardtii.–J. Biol. Chem. 273: 29315–29320, 1998.CrossRefPubMedGoogle Scholar
  27. Müh F., Glöckner C., Hellmich J. et al.: Light-induced quinone reduction in photosystem II.–Biochim. Biophys. Acta 1817: 44–65, 2012.CrossRefPubMedGoogle Scholar
  28. Mullineaux C.W., Allen J.F.: State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II.–Photosynth. Res. 23: 297–311, 1990.CrossRefPubMedGoogle Scholar
  29. Murchie E.H., Niyogi K.K.: Manipulation of photoprotection to improve plant photosynthesis.–Plant Physiol. 155: 86–92, 2011.CrossRefPubMedGoogle Scholar
  30. Page L.E., Liberton M., Pakrasi H.B.: Reduction of photoautotrophic productivity in the cyanobacterium Synechocystis sp. strain PCC 6803 by phycobilisome antenna truncation.–Appl. Environ. Microbiol. 78: 6349–6351, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pakrasi H.B., Williams J.G., Arntzen C.J.: Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b559 in photosystem II.–EMBO J. 7: 325–332, 1988.PubMedPubMedCentralGoogle Scholar
  32. Shinopoulos K.E., Brudvig G.W.: Cytochrome b559 and cyclic electron transfer within photosystem II.–Biochim. Biophys. Acta 1817: 66–75, 2012.CrossRefPubMedGoogle Scholar
  33. Stephenson P.G., Moore C.M., Terry M.J. et al.: Improving photosynthesis for algal biofuels: toward a green revolution.–Trends Biotechnol. 29: 615–623, 2011.CrossRefPubMedGoogle Scholar
  34. Stewart D.H., Brudvig G.W.: Cytochrome b559 of photosystem II.–BBA-Bioenergetics 1367: 63–87, 1998.CrossRefPubMedGoogle Scholar
  35. Suga M., Akita F., Hirata K. et al.: Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond Xray pulses.–Nature 517: 99–103, 2015.CrossRefPubMedGoogle Scholar
  36. Umena Y., Kawakami K., Shen J.R. et al.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.–Nature 473: 55–60, 2011.CrossRefPubMedGoogle Scholar
  37. Whitmarsh J., Pakrasi H.B.: Form and function of cytochrome b559.–In: Ort D.R., Yocum C.F., Heichel I.F. (ed.): Oxygenic photosynthesis: The Light Reactions. Pp. 249–264. Springer, Dordrecht 1996.Google Scholar
  38. Wilhelm C., Selmar D.: Energy dissipation is an essential mecha nism to sustain the viability of plants: The physiological limits of improved photosynthesis.–J. Plant Physiol. 168: 79–87, 2011.CrossRefPubMedGoogle Scholar
  39. Wilson A., Ajlani G., Verbavatz J.M. et al: A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria.–Plant Cell 18: 992–1007, 2006.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • J.-Y. Huang
    • 1
  • N.-T. Hung
    • 1
  • K.-M. Lin
    • 1
  • Y.-F. Chiu
    • 1
  • H.-A. Chu
    • 1
  1. 1.Institute of Plant and Microbial BiologyAcademia SinicaTaipeiTaiwan

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