Skip to main content

Composition and functional property of photosynthetic pigments under circadian rhythm in the cyanobacterium Spirulina platensis

Abstract

Circadian rhythm is an important endogenous biological signal for sustainable growth and development of cyanobacteria in natural ecosystems. Circadian effects of photosynthetically active radiation (PAR), ultraviolet-A (UV-A) and ultraviolet-B (UV-B) radiations on pigment composition have been studied in the cyanobacterium Spirulina platensis under light (L)/dark (D) oscillation with a combination of 4/20, 8/16, 12/12, 16/8, 20/4 and 24/24 h time duration. Circadian exposure of PAR + UV-A (PA) and PAR + UV-A + UV-B (PAB) showed more than twofold decline in Chl a, total protein and phycocyanin (PC) in light phase and significant recovery was achieved in dark phase. The fluorescence emission wavelength of PC was shifted towards lower wavelengths in the light phase of PAB in comparison to P and PA whereas the same wavelength was retrieved in the dark phase. The production of free radicals was accelerated twofold in the light phase (24 h L) whereas the same was retrieved to the level of control during the dark phase. Oxidatively induced damage was alleviated by antioxidative enzymes such as catalase (CAT), peroxidase (POD), superoxide dismutase (SOD) and ascorbate peroxidase (APX) in the light phase (0–24-h L) whereas the dark phase showed significant inhibition of the same enzymes. Similar characteristic inhibition of free radicals and recovery of PC was observed inside cellular filament after circadian rhythm of 24/24 h (L/D). Circadian exposure of P, PA and PAB significantly altered the synthesis and recovery of pigments that could be crucial for optimization and sustainable production of photosynthetic products for human welfare.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

DCFH-DA:

2′,7′-Dichlorodihydrofluorescein diacetate

L:

Light

D:

Dark

PBPs:

Phycobiliproteins

PBSs:

Phycobilisomes

PC:

Phycocyanin

PE:

Phycoerythrin

P:

Photosynthetically active radiation

POD:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

UV-A:

Ultraviolet-A

UV-B:

Ultraviolet-B

References

  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3

    CAS  Article  PubMed  Google Scholar 

  3. Ballaré CL, Caldwell MM, Flint SD, Robinson SA, Bornman JF (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems patterns, mechanisms, and interactions with climate change. Photochem Photobiol Sci 10(2):226–241. https://doi.org/10.1039/c0pp90035d

    Article  PubMed  Google Scholar 

  4. Beauchamp C, Fridovich I (1971) Superoxide dismutase:improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287. https://doi.org/10.1016/0003-2697(71)90370-8

    CAS  Article  PubMed  Google Scholar 

  5. Bhandari R, Sharma PK (2006) High-light-induced changes on photosynthesis, pigments, sugars, lipids and antioxidant enzymes in freshwater (Nostoc spongiaeforme) and marine (Phormidium corium) cyanobacteria. Photochem Photobiol 82(3):702–710. https://doi.org/10.1562/2005-09-20-RA-690

    CAS  Article  PubMed  Google Scholar 

  6. Britton C, Mehley AC (1955) Assay of catalase and peroxidase. In: Colowick SP, Kalpan NO (eds) Method in enzymology. Academic, New York, pp 764–775

    Google Scholar 

  7. Bryant DA, Guglielmi G, Tandeau de Marsac N, Castlets AM, Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisomes:a model. Arch Microbiol 123(2):113–127. https://doi.org/10.1007/BF00446810

    CAS  Article  Google Scholar 

  8. Chis C, Druga B, Carmel AD, Chis I, Ardelean A, Sicora CI (2016) UV-B stress changes the electron flow on photosystem II complex in Synechococcus sp. PCC 7002. Rom. Biotechnol Lett 22:12142–12146

    Google Scholar 

  9. Chukhutsina V, Bersanini L, Aro E-M, van Amerongen H (2015) Cyanobacterial light-harvesting phycobilisomes uncouple from photosystem I during dark-to-light transitions. Sci Rep 5(1):14193. https://doi.org/10.1038/srep14193

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Cohen SE, Golden SS (2015) Circadian rhythms in cyanobacteria. Microbiol Mol Biol Rev 79(4):373–385. https://doi.org/10.1128/MMBR.00036-15

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Dere S, Günes T, Sivaci R (1998) Spectrophotometric determination of chlorophyll-A, B and total carotenoid contents of some algae species using different solvents. Turk J Bot 22:13–17

    Google Scholar 

  12. Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defense against lipid peroxidation. J Exp Bot 32(1):79–91. https://doi.org/10.1093/jxb/32.1.79

    CAS  Article  Google Scholar 

  13. Dong G, Golden SS (2008) How a cyanobacterium tells time. Curr Opin Microbiol 11:541–546

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Fischer WF (2008) Life before the rise of oxygen. Nature 455(7216):1051–1052. https://doi.org/10.1038/4551051a

    CAS  Article  PubMed  Google Scholar 

  15. Fragoso GM, Neale PJ, Kana TM, Pritchard AL (2014) Kinetics of photosynthetic response to ultraviolet and photosynthetically active radiation in Synechococcus WH8102 (cyanobacteria). Photochem Photobiol 90(3):522–532. https://doi.org/10.1111/php.12202

    CAS  Article  PubMed  Google Scholar 

  16. Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39(7):1704–1717. https://doi.org/10.4319/lo.1994.39.7.1704

    Article  Google Scholar 

  17. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990(1):87–92. https://doi.org/10.1016/S0304-4165(89)80016-9

    CAS  Article  Google Scholar 

  18. Grossman AR, Schaefer M, Chiang GG, Collier JL (1993) The phycobilisome, a light harvesting complex responsive to environmental conditions. Microbiol Rev 57(3):725–749

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Häder D-P, Williamson CE, Wängberg S, Rautio M, Rose KC, Gao K, Helbling EW, Sinha RP, Worrest R (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14(1):108–126. https://doi.org/10.1039/C4PP90035A

    Article  PubMed  Google Scholar 

  20. Halliwell B (2006) Reactive species and antioxidants:redox biology is a fundamental theme of aerobic life. Plant Physiol 141(2):312–322. https://doi.org/10.1104/pp.106.077073

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Hargreaves A, Taiwo FA, Duggan O, Kirk SH, Ahmad SI (2007) Near ultraviolet photolysis of β -phenylpyruvic acid generates free radicals and results in DNA damage. J Photochem Photobiol B Biol 89(2-3):110–116. https://doi.org/10.1016/j.jphotobiol.2007.09.007

    CAS  Article  Google Scholar 

  22. He Y-Y, Häder D-P (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol B Bio 66(2):115–124. https://doi.org/10.1016/S1011-1344(02)00231-2

    CAS  Article  Google Scholar 

  23. Helbling W, Gao K, Ai H, Ma Z, Villafañe VE (2006) Differential responses of Nostoc sphaeroides and Arthrospira platensis to solar ultraviolet radiation exposure. J Appl Phycol 18(1):57–66. https://doi.org/10.1007/s10811-005-9015-5

    Article  Google Scholar 

  24. Hurley JM, Loros JJ, Dunlap JC (2016) Circadian oscillators: around the transcription-translation feedback loop and on to output. Trends Biochem Sci 41(10):834–846. https://doi.org/10.1016/j.tibs.2016.07.009

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Johnson CH (2007) Bacterial circadian programs. Cold Spring Harb Symp Quant Biol 72(1):395–404. https://doi.org/10.1101/sqb.2007.72.027

    CAS  Article  PubMed  Google Scholar 

  26. Kampfenkel K, Van Montagu M, Inzè D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225(1):165–167. https://doi.org/10.1006/abio.1995.1127

    CAS  Article  PubMed  Google Scholar 

  27. Kannaujiya VK, Sinha RP (2015) Impacts of varying light regimes on phycobiliproteins of Nostoc sp. HKAR-2 and Nostoc sp. HKAR-11 isolated from diverse habitats. Protoplasma 252(6):1551–1561. https://doi.org/10.1007/s00709-015-0786-5

    CAS  Article  PubMed  Google Scholar 

  28. Kannaujiya VK, Sinha RP (2016a) Thermokinetic stability of phycocyanin and phycoerythrin in food-grade preservatives. J Appl Phycol 28(2):1063–1070. https://doi.org/10.1007/s10811-015-0638-x

    CAS  Article  Google Scholar 

  29. Kannaujiya VK, Sinha RP (2016b) An efficient method for separation and purification of phycobiliproteins from rice-field cyanobacterium Nostoc sp. strain HKAR-11. Chromatographia 79(5-6):335–343. https://doi.org/10.1007/s10337-016-3025-0

    CAS  Article  Google Scholar 

  30. Kannaujiya VK, Sinha RP (2017a) Impacts of diurnal variation of ultraviolet-B and photosynthetically active radiation on phycobiliproteins of the hot-spring cyanobacterium Nostoc sp. strain HKAR-2. Protoplasma 254(1):423–433. https://doi.org/10.1007/s00709-016-0964-0

    CAS  Article  PubMed  Google Scholar 

  31. Kannaujiya VK, Sinha RP (2017b) Detection of free thiols and fluorescence response of phycoerythrin chromophore after ultraviolet-B radiation stress. J Fluoresc 27(2):561–567. https://doi.org/10.1007/s10895-016-1983-0

    CAS  Article  PubMed  Google Scholar 

  32. Kannaujiya VK, Rastogi RP, Sinha RP (2014a) GC constituents and relative codon expressed amino acid composition in cyanobacterial phycobiliproteins. Gene 546(2):162–171. https://doi.org/10.1016/j.gene.2014.06.024

    CAS  Article  PubMed  Google Scholar 

  33. Kannaujiya VK, Richa, Sinha RP (2014b) Peroxide scavenging potential of ultraviolet-B-absorbing mycosporine-like amino acids isolated from a marine red alga Bryocladia sp. Front Environ Sci 2:26

    Article  Google Scholar 

  34. Karsten U, Lembcke S, Schumann R (2007) The effects of ultraviolet radiation on photosynthetic performance, growth and sunscreen compounds in aero terrestrial biofilm algae isolated from building facades. Planta 225(4):991–1000. https://doi.org/10.1007/s00425-006-0406-x

    CAS  Article  PubMed  Google Scholar 

  35. Khajepour F, Hosseini SA, Nasrabadi RG, Markou G (2015) Effect of light intensity and photoperiod on growth and biochemical composition of a local isolate of Nostoc calcicola. Appl Biochem Biotechnol 176(8):2279–2289. https://doi.org/10.1007/s12010-015-1717-9

    CAS  Article  PubMed  Google Scholar 

  36. Kim YI, Vinyard DJ, Ananyev GM, Dismukes GC, Golden SS (2012) Oxidized quinones signal onset of darkness directly to the cyanobacterial circadian oscillator. Proc Natl Acad Sci U S A 109:17765–17769

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B Biol 137:89–99. https://doi.org/10.1016/j.jphotobiol.2014.02.016

    CAS  Article  Google Scholar 

  38. Lao K, Glazer AN (1996) Ultraviolet-B destruction of a light harvesting complex. Proc Natl Acad Sci U S A 93(11):5258–5263. https://doi.org/10.1073/pnas.93.11.5258

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33(2):258–278. https://doi.org/10.1111/j.1574-6976.2008.00134.x

    CAS  Article  PubMed  Google Scholar 

  40. Lee T-M, Shiu C-T (2009) Implications of mycosporine-like amino acid and antioxidant defenses in UV-B radiation tolerance for the algae species Ptercladiella capillacea and Gelidium amansii. Mar Environ Res 67(1):8–16. https://doi.org/10.1016/j.marenvres.2008.09.006

    CAS  Article  PubMed  Google Scholar 

  41. Lowry HO, Rosenbrough NJ, Farr AL, Randell RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  42. Lu C, Vonshak A (1999) Photoinhibition in outdoor Spirulina platensis cultures assessed by polyphasic chlorophyll fluorescence transients. J Appl Phycol 11(4):355–359. https://doi.org/10.1023/A:1008195927725

    Article  Google Scholar 

  43. Maniscalco M, Nannen J, Sodi V, Silver G, Lowrey PL, Bidle KA (2014) Light-dependent expression of four cryptic archaeal circadian gene homologs. Front Microbiol 5:79

    Article  PubMed  PubMed Central  Google Scholar 

  44. Marwood CA, Greenberg BM (1996) Effect of supplementary UV-B radiation on chlorophyll synthesis and accumulation of photosystems during chloroplast development in Spirodela oligorrhiza. Photochem Photobiol 64(4):664–670. https://doi.org/10.1111/j.1751-1097.1996.tb03121.x

    CAS  Article  Google Scholar 

  45. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H, Oyama T, Kondo T (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308(5720):414–415. https://doi.org/10.1126/science.1108451

    CAS  Article  PubMed  Google Scholar 

  46. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  47. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95(15):8660–8664. https://doi.org/10.1073/pnas.95.15.8660

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Pattanaik B, Roleda MY, Schumann R, Karsten U (2008) Isolate-specific effects of ultraviolet radiation on photosynthesis, growth and mycosporine-like amino acids in the microbial mat-forming cyanobacterium Microcoleus chthonoplastes. Planta 227(4):907–916. https://doi.org/10.1007/s00425-007-0666-0

    CAS  Article  PubMed  Google Scholar 

  49. Polo LK, de Marthiellen LFR, Kreusch M, Pereira DT, Costa GB, Simioni C, Ouriques LC, Chow F, Ramlov F, Maraschin M, Bouzon ZL, Schmidt EC (2014) Photo acclimation responses of the brown macroalga Sargassum cymosum to the combined influence of UV radiation and salinity: cytochemical and ultrastructural organization and photosynthetic performance. Photochem Photobiol 90(3):560–573. https://doi.org/10.1111/php.12224

    CAS  Article  PubMed  Google Scholar 

  50. Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787(10):1151–1160. https://doi.org/10.1016/j.bbabio.2009.05.005

    Article  PubMed  Google Scholar 

  51. Rastogi RP, Singh SP, Häder D-P, Sinha RP (2010) Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937. Biochem Biophys Res Commun 397(3):603–607. https://doi.org/10.1016/j.bbrc.2010.06.006

    CAS  Article  PubMed  Google Scholar 

  52. Rastogi RP, Incharoensakdi A, Madamwar D (2014) Responses of a rice-field cyanobacterium Anabaena siamensis TISTR-8012 upon exposure to PAR and UV radiation. J Plant Physio 171(16):1545–1553. https://doi.org/10.1016/j.jplph.2014.07.011

    CAS  Article  Google Scholar 

  53. Rastogi RP, Sonani RR, Madamwar D (2015) Effects of PAR and UV radiation on the structural and functional integrity of phycocyanin, phycoerythrin and allophycocyanin isolated from the marine cyanobacterium Lyngbya sp. A09DM. Photochem Photobiol 91(4):837–844. https://doi.org/10.1111/php.12449

    CAS  Article  PubMed  Google Scholar 

  54. Rastogi RP, Sonani RR, Madamwar D, Incharoensakdi A (2016) Characterization and antioxidant functions of mycosporine-like amino acids in the cyanobacterium Nostoc sp. R76DM. Algal Res 16:110–118. https://doi.org/10.1016/j.algal.2016.03.009

    Article  Google Scholar 

  55. Richa, Sinha RP (2015) Biochemical characterization of sun screening mycosporine-like amino acids from two Nostoc species inhabiting diverse habitats. Protoplasma 252(1):199–208. https://doi.org/10.1007/s00709-014-0674-4

    CAS  Article  PubMed  Google Scholar 

  56. Richa, Kannaujiya VK, Kesheri M, Singh G, Sinha RP (2011) Biotechnological potentials of phycobiliproteins. Int J Pharma Bio Sci 2:446–454

    CAS  Google Scholar 

  57. Santos AL, Moreirinha C, Lopes D, Esteves AC, Henriques I, Almeida A, Domingues MRM, Delgadillo I, Correia A, Cunha Ä (2013) Effects of UV Radiation on the lipids and proteins of bacteria studied by mid-infrared spectroscopy. Environ Sci Technol l47:6306–6315

    Article  Google Scholar 

  58. Sekar S, Chandramohan M (2008) Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. J Appl Phycol 20(2):113–136. https://doi.org/10.1007/s10811-007-9188-1

    Article  Google Scholar 

  59. Shiu CT, Lee TM (2005) Ultraviolet-B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata. J Exp Bot 56(421):2851–2865. https://doi.org/10.1093/jxb/eri277

    CAS  Article  PubMed  Google Scholar 

  60. Singh SP, Montgomery BL (2011) Determining cell shape: adaptive regulation of cyanobacterial cellular differentiation and morphology. Trends Microbiol 19(6):278–285. https://doi.org/10.1016/j.tim.2011.03.001

    CAS  Article  PubMed  Google Scholar 

  61. Singh SP, Rastogi RP, Sinha RP, Häder D-P (2013a) Photosynthetic performance of Anabaena variabilis PCC 7937 under simulated solar radiation. Photosynthetica 51(2):259–266. https://doi.org/10.1007/s11099-013-0012-7

    CAS  Article  Google Scholar 

  62. Singh G, Babele PK, Sinha RP, Tyagi MB, Kumar A (2013b) Enzymatic and non-enzymatic defense mechanisms against ultraviolet-B radiation in two Anabaena species. Process Biochem 48(5-6):796–802. https://doi.org/10.1016/j.procbio.2013.04.022

    CAS  Article  Google Scholar 

  63. Sinha RP, Häder D-P (1998) Effects of ultraviolet-B radiation in three rice-field cyanobacteria. J Plant Physiol 153(5-6):763–769. https://doi.org/10.1016/S0176-1617(98)80232-0

    CAS  Article  Google Scholar 

  64. Sinha RP, Lebert M, Kumar A, Kumar HD, Häder D-P (1995) Spectroscopic and biochemical analyses of UV effects on phycobiliproteins of Anabaena sp. and Nostoc carmium. Bot Acta 108(2):87–92. https://doi.org/10.1111/j.1438-8677.1995.tb00836.x

    CAS  Article  Google Scholar 

  65. Sinha RP, Richter P, Faddoul J, Braun M, Häder D-P (2002a) Effects of UV and visible light on cyanobacteria at the cellular level. Photochem Photobio Sci 1(8):553–559. https://doi.org/10.1039/B203955A

    CAS  Article  Google Scholar 

  66. Sinha RP, Gröniger A, Klisch M, Häder D-P (2002b) Ozone depletion and ultraviolet-B radiation: impacts on aquatic organism. Recent Res Devel Photochem Photobiol 6:95–106

    CAS  Google Scholar 

  67. Sinha RP, Barbieri ES, Lebert M, Helbling EW, Häder D-P (2003a) Effects of solar radiation on phycobiliproteins of marine red algae. Trends Photochem Photobiol 10:149–157

    CAS  Google Scholar 

  68. Sinha RP, Helbling EW, Häder D-P (2003b) Effects of solar radiation on photosynthetic quantum yield of a cyanobacterium Nostoc sp. Trends Photochem Photobiol 10:159–166

    CAS  Google Scholar 

  69. Six C, Joubin L, Partensky F, Holtzendorff J, Garczarek L (2007) UV induced phycobilisome dismantling in the marine picocyanobacterium Synechococcus sp. WH8102. Photosynth Res 92(1):75–86. https://doi.org/10.1007/s11120-007-9170-4

    CAS  Article  PubMed  Google Scholar 

  70. Sonani RR, Rastogi RP, Madamwar D (2015) Antioxidant potential of phycobiliproteins: role in anti-aging research. Biochem Anal Biochem 4:172

    Article  Google Scholar 

  71. Tandeau de Marsac N, Houmard J (1988) Complementary chromatic adaptation:physiological conditions and action spectra. Methods Enzymol 167:318–328. https://doi.org/10.1016/0076-6879(88)67037-6

    CAS  Article  Google Scholar 

  72. Teng SW, Mukherji S, Moffitt JR, de Buyl S, O’Shea EK (2013) Robust circadian oscillations in growing cyanobacteria require transcriptional feedback. Science 340:737–740

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Tripathi SN, Srivastava P (2001) Presence of stable active oxygen scavenging enzymes superoxide dismutase, ascorbate peroxidase and catalase in a desiccation-tolerant cyanobacterium Lyngbya arboricola under dry state. Curr Sci 81:197–200

    CAS  Google Scholar 

  74. van Kooten O, Snel JF (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Res 25(3):147–150. https://doi.org/10.1007/BF00033156

    Article  Google Scholar 

  75. Wu H, Gao K, Villafañe VE, Watanabe T, Helbling EW (2005) Effects of solar UV radiation and photosynthesis of the filamentous cyanobacterium, Arthrospira platensis. Appl Environ Microbiol 71(9):5004–5013. https://doi.org/10.1128/AEM.71.9.5004-5013.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. Young AJ (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83(4):702–708. https://doi.org/10.1111/j.1399-3054.1991.tb02490.x

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We are thankful to the Interdisciplinary School of Life Sciences (ISLS), BHU, Varanasi, India, for providing access to the fluorescence microscopy facility.

Funding

Deepak Kumar is thankful to the Department of Science and Technology, Inspire Program, New Delhi, India, for the financial assistance in the form of a junior research fellowship (DST/Inspire Fellowship/2015/IF150191). Vinod K. Kannaujiya is thankful to the University Grant Commission (UGC), New Delhi, India, for the Dr. D.S. Kothari Postdoctoral Research Grant (F.4-2/2006(BSR)/14-15/0526). Richa is thankful to the Department of Science and Technology, Govt. of India, New Delhi, for providing the financial support in the form of a fellowship under the project (No. SR/WOS-A/LS-140/2011). The Council of Scientific and Industrial Research, New Delhi, India, is thankfully acknowledged for the financial support in the form of a senior research fellowship (09/013/0515/2013-EMR-I) sanctioned to Jainendra Pathak.

Author information

Affiliations

Authors

Contributions

V.K. Kannaujiya designed the experiments, evaluated the results and wrote the manuscript. D. Kumar performed the experiments and analyzed data. Richa and J. Pathak performed writing and editing of the manuscript. S. Sundaram critically analyzed the manuscript. R.P. Sinha supervised the experiments and critically analyzed the manuscript.

Corresponding author

Correspondence to Rajeshwar P. Sinha.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Andreas Holzinger

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kumar, D., Kannaujiya, V.K., Richa et al. Composition and functional property of photosynthetic pigments under circadian rhythm in the cyanobacterium Spirulina platensis . Protoplasma 255, 885–898 (2018). https://doi.org/10.1007/s00709-017-1195-8

Download citation

Keywords

  • Antioxidative enzymes
  • Circadian rhythm
  • Free radicals
  • Phycocyanin
  • Ultraviolet radiation