In this work, we reconstructed the absorption spectrum of different Synechocystis sp. PCC 6803 optical strains by summing the computed signature of all pigments present in this organism. To do so, modifications to in vitro pigment spectra were first required: namely wavelength shift, curve smoothing, and the package effect calculation derived from high pigment densities were applied. As a result, we outlined a plausible shape for the in vivo absorption spectrum of each chromophore. These are flatter and slightly broader in physiological conditions yet the mean weight-specific absorption coefficient remains identical to the in vitro conditions. Moreover, we give an estimate of all pigment concentrations without applying spectrophotometric correlations, which are often prone to error. The computed cell spectrum reproduces in an accurate manner the experimental spectrum for all the studied wavelengths in the wild-type, Olive, and PAL strain. The gathered pigment concentrations are in agreement with reported values in literature. Moreover, different illumination set-ups were evaluated to calculate the mean absorption cross-section of each chromophore. Finally, a qualitative estimate of light-limited cellular growth at each wavelength is given. This investigation describes a novel way to approach the cell absorption spectrum and shows all its inherent potential for photosynthesis research.

Department of Adaptation Biotechnologies Global Change Research Centre Academy of Science of the Czech Republic Drásov Czech Republic

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Czech Republic

Department of Biophysics Faculty of Science Palacký University Olomouc Czech Republic

Instituto de Aplicaciones de las Tecnologías de la Información y de las Comunicaciones Avanzadas Universitat Politècnica de València Valencia Spain

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Aasen AJ, Liaaen Jensen S (1966) Carotenoids of flexibacteria. IV. The carotenoids of two further pigment types. Acta Chem Scand 20(8):2322–2324 PubMed

Ajlani G, Vernotte C (1998) Construction and characterization of a phycobiliprotein-less mutant of Synechocystis Sp. PCC 6803. Plant Mol Biol 37(3):577–580 PubMed

Bennett A, Bogobad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58(2):419–435 PubMed PMC

Bidigare RR, Ondrusek ME, Morrow JH, Kiefer DA (1990) In-Vivo Absorption Properties of Algal Pigments. In: Ocean Optics X, SPIE, 290. https://spie.org/Publications/Proceedings/Paper/10.1117/12.21451 . Accessed 31 March 2020

Bricaud A, Stramski D (1990) Spectral absorption coefficients of living phytoplankton and nonalgal biogenous matter: a comparison between the peru upwelling areaand the Sargasso Sea. Limnol Oceanogr 35(3):562–582

Bricaud A, Claustre H, Ras J, Oubelkheir K (2004) Natural variability of phytoplanktonic absorption in oceanic waters: influence of the size structure of algal populations. J Geophys Res 109:C11010

Bryant DA, Glazer AN, Eiserling FA (1976) Characterization and structural properties of the major biliproteins of Anabaena Sp. Arch Microbiol 110(1):61–75 PubMed

Buschmann C, Nagel E (1993) In vivo spectroscopy and internal optics of leaves as basis for remote sensing of vegetation. Int J Remote Sens 14(4):711–722

Cerullo G et al (2002) Photosynthetic light harvesting by carotenoids: detection of an intermediate excited state. Science 298(5602):2395–2398 PubMed

Chábera P et al (2011) Excited-state properties of the 16kDa red carotenoid protein from arthrospira maxima. Biochimica et Biophysica Acta - Bioenergetics 1807(1):30–35

Collins AM et al (2012) Photosynthetic pigment localization and thylakoid membrane morphology are altered in Synechocystis 6803 phycobilisome mutants. Plant Physiol 158(4):1600–1609 PubMed PMC

de Mooij T et al (2016) Impact of light color on photobioreactor productivity. Algal Res 15:32–42

Eng D, Baranoski GVG (2007) The application of photoacoustic absorption spectral data to the modeling of leaf optical properties in the visible range. In: IEEE transactions on geoscience and remote sensing, pp 4077–4086. https://ieeexplore.ieee.org/document/4378552 . Accessed 31 March 2020

Faccio G et al (2014) Tyrosinase-catalyzed site-specific immobilization of engineered C-phycocyanin to surface. Sci Rep 4:5370 PubMed PMC

Ficek D et al (2004) Spectra of light absorption by phytoplankton pigments in the Baltic; conclusions to be drawn from a Gaussian analysis of empirical data. Oceanologia 46(4):533–555

Fuente D et al (2017) Light distribution and spectral composition within cultures of micro-algae: quantitative modelling of the light field in photobioreactors. Algal Res 23

Fujiki T, Taguchi S (2002) Variability in Chlorophyll a specific absorption coefficient in marine phytoplankton as a function of cell size and irradiance. J Plankton Res 24(9):859–874

Gobets B, Van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507(1–3):80–99 PubMed

Gobets B et al (2003) Excitation wavelength dependence of the fluorescence kinetics in photosystem I particles from Synechocystis PCC 6803 and Synechococcus Elongatus. Biophys J 85(6):3883–3898 PubMed PMC

Gong N, Li Z, Sun C, Men Z (2018) External field effect on electronic and vibrational properties of carotenoids. In: Progress in carotenoid research. InTech. https://www.intechopen.com/books/progress-in-carotenoid-research/external-field-effect-on-electronic-and-vibrational-properties-of-carotenoids . Accessed 31 March 2020

Green BR, Parson WW (2003) Light-harvesting antennas in photosynthesis. Adv Photosynth Resp 13:513

Greg Mitchell B, Kiefer DA (1988) Chlorophyll α specific absorption and fluorescence excitation spectra for light-limited phytoplankton. Deep Sea Res A 35(5):639–663

Herbert SK, Han T, Vogelmann TC (2000) New applications of photoacoustics to the study of photosynthesis. Photosynth Res 66(1–2):13–31 PubMed

Hertzberg S, Liaaen-Jensen S, Siegelman HW (1971) The carotenoids of blue-green algae. Phytochemistry 10(12):3121–3127

Hiyama T, Nishimura M, Chance B (1969) Determination of carotenes by thin-layer chromatography. Anal Biochem 29(2):339–342 PubMed

Hoepffner N, Sathyendranath S (1991) Effect of pigment composition on absorption properties of phytoplankton. Mar Ecol Prog Ser 73:11–23

Jordan P et al (2001) Three-dimensional structure of cyanobaoterial photosystem I at 2.5 Å resolution. Nature 411(6840):909–917 PubMed

Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135(4):2112–2119 PubMed PMC

Kakitani T, Honig B, Crofts AR (1982) Theoretical studies of the electrochromic response of carotenoids in photosynthetic membranes. Biophys J 39(1):57–63 PubMed PMC

Kilian O et al (2007) Responses of a thermophilic synechococcus isolate from the microbial mat of octopus spring to light. Appl Environ Microbiol 73(13):4268–4278 PubMed PMC

Kłodawska K et al (2015) Elevated growth temperature can enhance photosystem I trimer formation and affects xanthophyll biosynthesis in cyanobacterium Synechocystis Sp. PCC6803 Cells. Plant Cell Physiol 56(3):558–571 PubMed

Knoop H, Zilliges Y, Lockau W, Steuer R (2010) The metabolic network of Synechocystis Sp. PCC 6803: systemic properties of autotrophic growth. Plant Physiol 154(1):410–422 PubMed PMC

Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144(2):1200–1210 PubMed PMC

Kopečná J, Komenda J, Bučinská L, Sobotka R (2012) Long-term acclimation of the cyanobacterium Synechocystis Sp. PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric photosystem I. Plant Physiol 160(4):2239–2250 PubMed PMC

Kwon J-H, Rögner M, Rexroth S (2012) Direct approach for bioprocess optimization in a continuous flat-bed photobioreactor system. J Biotechnol 162(1):156–162 PubMed

Kwon JH et al (2013) Reduced light-harvesting antenna: consequences on cyanobacterial metabolism and photosynthetic productivity. Algal Res 2(3):188–195

Lagarde D, Vermaas W (1999) The zeaxanthin biosynthesis enzyme β-carotene hydroxylase is involved in myxoxanthophyll synthesis in Synechocystis Sp. PCC 6803. FEBS Lett 454(3):247–251 PubMed

Lauceri R, Bresciani M, Lami A, Morabito G (2018) Chlorophyll a interference in phycocyanin and allophycocyanin spectrophotometric quantification. J Limnol 77(1):169–177

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148(C):350–382

Lindblad P et al (2019) CyanoFactory, a European Consortium to develop technologies needed to advance cyanobacteria as chassis for production of chemicals and fuels. Algal Res 41:101510

Liu H et al (2019) Phycobilisomes harbor FNRL in cyanobacteria. mBio 10: e00669–19.

Luimstra VM et al (2018) Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II. Photosynth Res 138(2):177–189 PubMed PMC

Luimstra VM et al (2019) Exploring the low photosynthetic efficiency of cyanobacteria in blue light using a mutant lacking phycobilisomes. Photosynth Res 141(3):291–301 PubMed PMC

Ma W, Ogawa T, Shen Y, Mi H (2007) Changes in cyclic and respiratory electron transport by the movement of phycobilisomes in the cyanobacterium Synechocystis Sp. Strain PCC 6803. Biochem Biophys Acta 1767(6):742–749 PubMed

MacColl R (2004) Allophycocyanin and energy transfer. Biochem Biophys Acta 1657(2–3):73–81 PubMed

Manodori A, Melis A (1986) Cyanobacterial acclimation to photosystem I or photosystem II light. Plant Physiol 82(1):185–189 PubMed PMC

McGee D et al (2020) Influence of spectral intensity and quality of LED lighting on photoacclimation, carbon allocation and high-value pigments in microalgae. Photosynth Res 143(1):67–80 PubMed

Moal G, Lagoutte B (2012) Photo-induced electron transfer from photosystem i to NADP+: characterization and tentative simulation of the in vivo environment. Biochem Biophys Acta 1817(9):1635–1645 PubMed

Morel A, Bricaud A (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Res Part A 28(11):1375–1393

Münzner P, Voigt J (1992) Blue light regulation of cell division in chlamydomonas reinhardtii. Plant Physiol 99(4):1370–1375 PubMed PMC

Orr L, Govindjee (2013) Photosynthesis web resources. Photosynth Res 115(2–3):179–214 PubMed

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. BBA 975(3):384–394

Rabe AE, Benoit RJ (1962) Mean light intensity—a useful concept in correlating growth rates of dense cultures of microalgae. Biotechnol Bioeng 4(4):377–390

Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium spirulina platensis. Biochemistry 40(51):15780–15788 PubMed

Remelli W, 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. Biochem Biophys Acta 1859(11):1207–1222

Rögner M, Nixon PJ, Diner BA (1990) Purification and characterization of photosystem I and photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium synechocystis PCC 6803. J Biol Chem 265(11):6189–6196 PubMed

Simis SGH, Kauko HM (2012) In vivo mass-specific absorption spectra of phycobilipigments through selective bleaching. Limnol Oceanogr 10(4):214–226

Singh AK et al (2009) A systems-level analysis of the effects of light quality on the metabolism of a cyanobacterium. Plant Physiol 151(3):1596–1608 PubMed PMC

Stirbet A, Lazár D, Papageorgiou GC, Govindjee (2019) Chlorophyll a fluorescence in cyanobacteria: relation to photosynthesis. In: Cyanobacteria. Elsevier, pp 79–130

Stramski D, Morel A (1990) Optical properties of photosynthetic picoplankton in different physiological states as affected by growth irradiance. Deep Sea Res A 37(2):245–266

Takaichi S, Maoka T, Masamoto K (2001) Myxoxanthophyll in Synechocystis Sp. PCC 6803 is myxol 2′-dimethyl-fucoside, (3R,2′S)-myxol 2′-(2,4-Di-O-methyl-α-l-fucoside), not rhamnoside. Plant Cell Physiol 42(7):756–762 PubMed

Thrane J-E et al (2015) Spectrophotometric analysis of pigments: a critical assessment of a high-throughput method for analysis of algal pigment mixtures by spectral deconvolution, ed. Schmitt FG. PLOS ONE 10(9): e0137645

Tian L et al (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133(45):18304–18311 PubMed

Touloupakis E, Cicchi B, Torzillo G (2015) A bioenergetic assessment of photosynthetic growth of Synechocystis Sp. PCC 6803 in continuous cultures. Biotechnol Biofuels 8(1):133 PubMed PMC

Tsunoyama Y et al (2009) Multiple rieske proteins enable short- and long-term light adaptation of Synechocystis Sp. PCC 6803. J Biol Chem 284(41):27875–27883 PubMed PMC

Tyystjärvi T et al (2002) Action spectrum of PsbA gene transcription is similar to that of photoinhibition in Synechocystis Sp. PCC 6803. FEBS Lett 516(1–3):167–171 PubMed

Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature 473(7345):55–60 PubMed

Vajravel S et al (2016) β-Carotene influences the phycobilisome antenna of cyanobacterium Synechocystis Sp. PCC 6803. Photosynth Res 130(1–3):403–415 PubMed

van Amerongen H, van Grondelle R, Valkunas L (2000) Photosynthetic excitons. World Scientific. https://www.worldscientific.com/worldscibooks/10.1142/3609 . Accessed 28 March 2020

von Wobeser EA et al (2011) Concerted changes in gene expression and cell physiology of the cyanobacterium Synechocystis sp. strain PCC 6803 during transitions between nitrogen and light-limited growth. Plant Physiol 155(3):1445–1457

Warren CK, Weedon BCL (1958) 804. Carotenoids and related compounds. Part VII. Synthesis of canthaxanthin and echinenone. J Chem Soc (Resumed) 3986–393.

Westermark S, Steuer R (2016) Toward multiscale models of cyanobacterial growth: a modular approach. Front Bioeng Biotechnol 4(DEC)

Woźniak B et al (2003) Modelling light and photosynthesis in the marine environment. Oceanologia 45(2):171–245

Wright SW, Jeffrey SW, Mantoura RFC (1997) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris

Yacobi YZ, Köhler J, Leunert F, Gitelson A (2015) Phycocyanin-specific absorption coefficient: eliminating the effect of chlorophylls absorption. Limnol Oceanogr 13(4):e10015

Zakar T et al (2017) Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis Sp PCC6803. Biochem Biophys Acta 1858(5):337–350

Zavřel T et al (2015) Characterization of a model cyanobacterium Synechocystis Sp. PCC 6803 autotrophic growth in a flat-panel photobioreactor. Eng Life Sci 15(1):122–132

Zavřel T, Očenášová P, Červený J (2017) Phenotypic characterization of Synechocystis Sp. PCC 6803 substrains reveals differences in sensitivity to abiotic stress, ed. Jacobs JM. PLOS ONE 12(12): e0189130

Zhang Y et al (2017) An extended PROSPECT: advance in the leaf optical properties model separating total chlorophylls into chlorophyll a and B. Sci Rep 7:6429 PubMed PMC

Zhao W, Xie J, Xiuling Xu, Zhao J (2015) State transitions and fluorescence quenching in the cyanobacterium Synechocystis PCC 6803 in response to changes in light quality and intensity. J Photochem Photobiol B 142:169–177 PubMed

Zlenko DV et al (2019) Role of the PB-LOOP in ApcE and phycobilisome core function in cyanobacterium Synechocystis Sp PCC 6803. Biochim Biophys Acta 1860(2):155–166

Shedding light on blue-green photosynthesis: A wavelength-dependent mathematical model of photosynthesis in Synechocystis sp. PCC 6803

Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis

Structures of a phycobilisome in light-harvesting and photoprotected states