Photosynthetica 2018, 56(1):192-199 | DOI: 10.1007/s11099-018-0765-0
Regulating photoprotection improves photosynthetic growth and biomass production in QC-site mutant cells of the cyanobacterium Synechocystis sp. PCC 6803
- 1 Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
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.
Keywords: cytochrome b559; photosynthesis; photosystem II; photoprotection; QC
Received: April 29, 2017; Accepted: September 5, 2017; Published: March 1, 2018Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- 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. Go to original source...
- 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. Go to original source...
- Bondarava N., Gross C.M., Mubarakshina M. et al.: Putative function of cytochrome b559 as a plastoquinol oxidase.-Physiol. Plantarum 138: 463-473, 2010. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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.
- 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. Go to original source...
- 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.
- 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. Go to original source...
- 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.
- 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. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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, 200 Go to original source...
- 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. Go to original source...
- 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.
- Kirilovsky D.: Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions.-Photosynth. Res. 126: 3-17, 2015. Go to original source...
- Kirilovsky D., Kerfeld C.A.: Cyanobacterial photoprotection by the orange carotenoid protein.-Nat. Plants 2: 16180, 2016. doi: 10.1038/nplants.2016.180 Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- Kromdijk J., Głowacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection.-Science 354: 857-861, 2016. Go to original source...
- Kruk J., Strzałka K.: Redox changes of cytochrome b559 in the presence of plastoquinones.-J. Biol. Chem. 276: 86-91, 2001. Go to original source...
- 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. Go to original source...
- Machado I.M., Atsumi S.: Cyanobacterial biofuel production.-J. Biotechnol. 162: 50-56, 2012. Go to original source...
- 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. Go to original source...
- Müh F., Glöckner C., Hellmich J. et al.: Light-induced quinone reduction in photosystem II.-Biochim. Biophys. Acta 1817: 44-65, 2012.
- 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. Go to original source...
- Murchie E.H., Niyogi K.K.: Manipulation of photoprotection to improve plant photosynthesis.-Plant Physiol. 155: 86-92, 2011. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- Shinopoulos K.E., Brudvig G.W.: Cytochrome b559 and cyclic electron transfer within photosystem II.-Biochim. Biophys. Acta 1817: 66-75, 2012.
- 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. Go to original source...
- Stewart D.H., Brudvig G.W.: Cytochrome b559 of photosystem II.-BBA-Bioenergetics 1367: 63-87, 1998. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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. Go to original source...
- 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. Go to original source...