Abstract
Cyanobacteria acclimate and adapt to changing light conditions by controlling the energy transfer between photosystem I (PSI) and II (PSII) and pigment composition. Photosynthesis is driven by balancing the excitation between PSI and PSII. To predict the detailed electron transfer flux of cyanobacteria, we refined the photosynthesis-related reactions in our previously reconstructed genome-scale model. Two photosynthetic bacteria, Arthrospira and Synechocystis, were used as models. They were grown under various spectral light conditions and flux balance analysis (FBA) was performed using photon uptake fluxes into PSI and PSII, which were converted from each light spectrum by considering the photoacclimation of pigments and the distribution ratio of phycobilisome to PSI and PSII. In Arthrospira, the FBA was verified with experimental data using six types of light-emitting diodes (White, Blue, Green, Yellow, Red1, and Red2). FBA predicted the cell growth of Synechocystis for the LEDs, excepting Red2. In an FBA simulation, cells used respiratory terminal oxidases and two NADH dehydrogenases (NDH-1 and NDH-2) to balance the PSI and PSII excitations depending on the light conditions. FBA simulation with our refined model functionally implicated NDH-1 and NDH-2 as a component of cyclic electron transport in the varied light environments.
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Abbreviations
- ARTO:
-
Alternative respiratory oxidase
- Car:
-
Carotenoid
- CET:
-
Cyclic electron transport
- Chl:
-
Chlorophyll
- Cox:
-
aa3-type cytochrome c oxidase complex
- Cyd:
-
Cytochrome bd-quinol oxidase complex
- cyt:
-
b6f Cytochrome b6f complex
- FBA:
-
Flux balance analysis
- Fd:
-
Ferredoxin
- FNR ferredoxin:
-
NADP+ reductase
- LED:
-
Light-emitting diodes
- LET:
-
Linear electron transport
- NDH-1:
-
Type I NADH dehydrogenase
- NDH-2:
-
Type II NADH dehydrogenase
- PBS:
-
Phycobilisome
- Pc:
-
Plastocyanin
- PQ:
-
Plastoquinone
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- RTO:
-
Respiratory terminal oxidase
- SDH:
-
Succinate dehydrogenase
References
Akimoto S, Yokono M, Hamada F et al (2012) Adaptation of light-harvesting systems of Arthrospira platensis to light conditions, probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta 1817:1483–1489
Akimoto S, Yokono M, Aikawa S, Kondo A (2013) Modification of energy-transfer processes in the cyanobacterium, Arthrospira platensis, to adapt to light conditions, probed by time-resolved fluorescence spectroscopy. Photosynth Res 117:235–243
Battchikova N, Wei L, Du L et al (2011) Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. J Biol Chem 286:36992–37001
Becker SA, Feist AM, Mo ML et al (2007) Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Nat Protoc 2:727–738
Bernát G, Appel J, Ogawa T, Rögner M (2011) Distinct roles of multiple NDH-1 complexes in the cyanobacterial electron transport network as revealed by kinetic analysis of P700+ reduction in various ndh-deficient mutants of Synechocystis sp. strain PCC6803. J Bacteriol 193:292–295
Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98
Boyle NR, Morgan JA (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 3:4
Broddrick JT, Rubin BE, Welkie DG et al (2016) Unique attributes of cyanobacterial metabolism revealed by improved genome-scale metabolic modeling and essential gene analysis. Proc Natl Acad Sci USA 113:E8344–E8353
Burnap RL, Sherman LA (1991) Deletion mutagenesis in Synechocystis sp. PCC6803 indicates that the Mn-stabilizing protein of photosystem II is not essential for O2 evolution. Biochemistry 30:440–446
Chang RL, Ghamsari L, Manichaikul A et al (2011) Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol Syst Biol 7:518
Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431
Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336:330–334
Collins AM, Liberton M, Jones HDT et al (2012) Photosynthetic pigment localization and thylakoid membrane morphology are altered in Synechocystis 6803 phycobilisome mutants. Plant Physiol 158:1600–1609
Dall’Osto L, Bressan M, Bassi R (2015) Biogenesis of light harvesting proteins. Biochim Biophys Acta 1847:861–871
Duanmu D, Rockwell NC, Lagarias JC (2017) Algal light sensing and photoacclimation in aquatic environments. Plant Cell Environ 40:2558–2570
Feist AM, Herrgård MJ, Thiele I et al (2009) Reconstruction of biochemical networks in microorganisms. Nat Rev Microbiol 7:129–143
Fujimori T, Higuchi M, Sato H et al (2005) The mutant of sll1961, which encodes a putative transcriptional regulator, has a defect in regulation of photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 139:408–416
Fujisawa T, Narikawa R, Maeda SI et al (2017) Cyanobase: a large-scale update on its 20th anniversary. Nucleic Acids Res 45:D551–D554
Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347
Ghosh T, Bhayani K, Paliwal C et al (2016) Cyanobacterial pigments as natural anti-hyperglycemic agents: an in vitro study. Front Mar Sci 3:146
Glazer AN (1984) Phycobilisome a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768:29–51
Grossman AR, Bhaya D, Apt KE, Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu Rev Genet 29:231–288
Heirendt L, Arreckx S, Pfau T et al (2019) Creation and analysis of biochemical constraint-based models: the COBRA Toolbox v3.0. Nat Protoc 14:639–702
Hihara Y, Sonoike K, Ikeuchi M (1998) A novel gene, pmgA, specifically regulates photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803 in response to high light. Plant Physiol 117:1205–1216
Ho M-Y, Soulier NT, Canniffe DP et al (2017) Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr Opin Plant Biol 37:24–33
Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548
Howitt CA, Vermaas WFJ (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37:17944–17951
Howitt CA, Udall PK, Vermaas WFJ (1999) Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. Strain PCC 6803 are involved in regulation rather than respiration. J Bacteriol 181:3994–4003
Huokko T, Muth-Pawlak D, Battchikova N et al (2017) Role of type 2 NAD(P)H dehydrogenase NdbC in redox regulation of carbon allocation in Synechocystis. Plant Physiol 174:1863–1880
Ikeuchi M, Tabata S (2001) Synechocystis sp. PCC 6803—a useful tool in the study of the genetics of cyanobacteria. Photosynth Res 70:73–83
Imam S, Schäuble S, Valenzuela J et al (2015) A refined genome-scale reconstruction of Chlamydomonas metabolism provides a platform for systems-level analyses. Plant J 84:1239–1256
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
Kawamura M, Mimuro M, Fujita Y (1979) Quantitative relationship between two reaction centers in the photosynthetic system of blue-green algae. Plant Cell Physiol 20:697–705
Kirilovsky D (2015) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126:3–17
Kirilovsky D, Kerfeld CA (2016) Cyanobacterial photoprotection by the orange carotenoid protein. Nat Plants 2:16180
Lea-Smith DJ, Ross N, Zori M et al (2013) Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol 162:484–495
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Mahadevan R, Schilling CH (2003) The effects of alternate optimal solutions in constrain-based genome-scale metabolic models. Metab Eng 5:264–276
Mimuro M, Kikuchi H (2003) Antenna systems and energy transfer in cyanophyta and rhodophyta. In: Green BR, Parson WW (eds) Light harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 281–306
Mitchell P (1975) The protonmotive Q cycle: a general formulation. FEBS Lett 59:137–139
Mullineaux CW (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res 95:175–182
Mullineaux CW (2014) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:7
Myers J, Graham J-R, Wang RT (1980) Light-harvesting in Anacystis nidulans studies in pigmant mutants. Plant Physiol 66:1144–1149
Nakajima T, Yoshikawa K, Toya Y et al (2017) Metabolic flux analysis of the Synechocystis sp. PCC 6803 ΔnrtABCD mutant reveals a mechanism for metabolic adaptation to nitrogen-limited conditions. Plant Cell Physiol 58:537–545
Nakamura Y, Kaneko T, Hirosawa M et al (1998) CyanoBase, a www database containing the complete nucleotide sequence of the genome of Synechocystis sp. strain PCC6803. Nucleic Acids Res 26:63–67
Nogales J, Gudmundsson S, Knight EM et al (2012) Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc Natl Acad Sci USA 109:2678–2683
Nomura CT, Persson S, Shen G et al (2006) Characterization of two cytochrome oxidase operons in the marine cyanobacterium Synechococcus sp. PCC 7002: inactivation of ctaDI affects the PS I:PS II ratio. Photosynth Res 87:215–228
Orth J, Thiele I, Palsson B (2010) What is flux balance analysis? Nat Biotechnol 28:245–248
Peltier G, Aro E-M, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu Rev Plant Biol 67:55–80
Pils D, Schmetterer G (2001) Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Microbiol Lett 203:217–222
Pils D, Gregor W, Schmetterer G (1997) Evidence for in vivo activity of three distinct respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC6803. FEMS Microbiol Lett 152:83–88
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394
Price ND, Reed JL, Palsson BØ (2004) Genome-scale models of microbial cells: evaluating the consequences of constraints. Nat Rev Microbiol 2:886–897
Qian X, Kim MK, Kumaraswamy GK et al (2017) Flux balance analysis of photoautotrophic metabolism: uncovering new biological details of subsystems involved in cyanobacterial photosynthesis. Biochim Biophys Acta Bioeng 1858:276–287
Rich PR (1988) A critical examination of the supposed variable proton stoichiometry of the chloroplast cytochrome bf complex. Biochim Biophys Acta 932:33–42
Rippka R, Deruelles J, Waterbury JB et al (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1–61
Rockwell NC, Duanmu D, Martin SS et al (2014) Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA 111:3871–3876
Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged. Proc Natl Acad Sci USA 97:14283–14288
Schilling C, Schuster S, Palsson BØ et al (1999) Metabolic pathway analysis: basic concepts and scientific applications in the post-genomic era. Biotechnol Prog 15:296–303
Schmetterer G, Alge D, Gregor W (1994) Deletion of cytochrome c oxidase genes from the cyanobacterium Synechocystis sp. PCC6803: evidence for alternative respiratory pathways. Photosynth Res 42:43–50
Schuller JM, Birrell JA, Tanaka H et al (2019) Structure adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer. Science 363:257–260
Shen G, Boussiba S, Vermaas WFJ (1993) Synechocystis sp. PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863
Sonani RR, Gardiner A, Rastogi RP et al (2018) Site, trigger, quenching mechanism and recovery of non-photochemical quenching in cyanobacteria: recent updates. Photosynth Res 137:171–180
Toyoshima M, Mori N, Moriyama T et al (2016) Analysis of triacylglycerol accumulation under nitrogen deprivation in the red alga Cyanidioschyzon merolae. Microbiology 162:803–812
Ungerer J, Lin PC, Chen HY, Pakrasi HB (2018) Adjustments to photosystem stoichiometry and electron transfer proteins are key to the remarkably fast growth of the cyanobacterium Synechococcus elongatus UTEX 2973. mBio 9:e002327–17
Vu TT, Stolyar SM, Pinchuk GE et al (2012) Genome-scale modeling of light-driven reductant partitioning and carbon fluxes in diazotrophic unicellular cyanobacterium Cyanothece sp. ATCC 51142. PLoS Comput Biol 8:e1002460
Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167:766–778
Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675
Yoshikawa K, Kojima Y, Nakajima T et al (2011) Reconstruction and verification of a genome-scale metabolic model for Synechocystis sp. PCC6803. Appl Microbiol Biotechnol 92:347–358
Yoshikawa K, Aikawa S, Kojima Y et al (2015) Construction of a genome-scale metabolic of Arthrospira platensis NIES-39 and metabolic design for cyanobacterial bioproduction. PLoS ONE 10:e0144430
Yoshikawa K, Toya Y, Shimizu H (2017) Metabolic engineering of Synechocystis sp. PCC 6803 for enhanced ethanol production based on flux balance analysis. Bioprocess Biosyst Eng 40:791–796
Yuan H, Cheung CYM, Hilbers PAJ, van Riel NAW (2016) Flux balance analysis of plant metabolism: the effect of biomass composition and model structure on model predictions. Front Plant Sci 7:537
Zakhartsev M, Medvedeva I, Orlov Y et al (2016) Metabolic model of central carbon and energy metabolisms of growing Arabidopsis thaliana in relation to sucrose translocation. BMC Plant Biol 16:262
Acknowledgements
This work was supported in part by Grants-in-Aid for Scientific Research (Grant Nos. 16H06552 and 16H06559).
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Toyoshima, M., Toya, Y. & Shimizu, H. Flux balance analysis of cyanobacteria reveals selective use of photosynthetic electron transport components under different spectral light conditions. Photosynth Res 143, 31–43 (2020). https://doi.org/10.1007/s11120-019-00678-x
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DOI: https://doi.org/10.1007/s11120-019-00678-x