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Efficacy of red light for enhanced cell disruption and fluorescence intensity of phycocyanin

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Abstract

In this study, red LED and urea used as light and nitrogen sources, respectively, for the cultivation of Spirulina to enhance the fluorescence property and purity of phycocyanin. Besides, there is a high concentration of phycocyanin leached out from red light (RL) grown cells than white light (WL) without cell disruption. This type of cultivation reduces the complexity of extraction methods and cost of the downstream process. The fluorescence intensity of C-PC enhanced while using red LEDs and purity ratio improved by single-step cation exchange chromatography. Phycocyanin from red-light-exposed culture exhibited pronounced antibacterial activity against bacteria. The hydrogen peroxide scavenging activity of C-PC (93.7%) is higher than the WL cultures (88.8%). Phycocyanin from RL culture exhibited a strong antiproliferative activity (64.1%) against HeLa cancer cell line. The present study aims to analyze the influence of red light and urea on enhancing the phycocyanin production.

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References

  1. Yalcin D, Katircioğlu HT, Özer T, Shamchi MP, Erkaya İA (2020) Evaluation of phytotherapeutic activities and phytochemical content of PhormidiumautumnaleGomont from natural freshwater sources. Environ Monit Assess 192(4):1–11

    Google Scholar 

  2. Zhang F, Man YB, Mo WY, Wong MH (2020) Application of Spirulina in aquaculture: a review on wastewater treatment and fish growth. Rev Aquac 12(2):582–599

    Google Scholar 

  3. Prasanna R, Sood A, Jaiswal P, Nayak S, Gupta V, Chaudhary V, Joshi M, Natarajan C (2010) Rediscovering cyanobacteria as valuable sources of bioactive compounds. Appl Biochem Microbiol 46:119–134

    CAS  Google Scholar 

  4. Bar-Eyal L, Shperberg-Avni A, Paltiel Y, Keren N, Adir N (2018) Light harvesting in cyanobacteria: the phycobilisomes. In: Croce R, Van Grondelle R, Van Amerongen H, Van Stokkum IHM (eds) Light harvesting in photosynthesis. Foundations of biochemistry and biophysics, 1st edn. CRC Press, Boca Raton, pp 77–93

    Google Scholar 

  5. Brain CM, Cladwell GS (2018) Method for the synthesis of phycocyanin, United States Patent No-20180155401A1.

  6. Ajayan KV, Selvaraju M, Thirugnanamoorthy K (2012) Enrichment of chlorophyll and phycobiliproteins in Spirulina platensis by the use of reflector light and nitrogen sources: An in-vitro study. Biomass Bioenerg 47:436–441

    CAS  Google Scholar 

  7. Prozyme (2009) C-phycocyanin (Specifications).Products USA

  8. Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    CAS  Google Scholar 

  9. Liu Y, Xu L, Cheng N, Lin L, Zhang C (2000) Inhibitory effects of phycocyanin from Spirulina platensis on the growth of human leukemia K562 cells. J Appl Phycol 12(2):125–130

    CAS  Google Scholar 

  10. Li B, Zhang X, Gao M, Chu X (2005) Effects of CD59 on antitumoral activities of phycocyanin from Spirulina platensis. Biomed Pharmaco 59(10):551–560

    CAS  Google Scholar 

  11. Romay CH, González R, Ledón N, Remirez D, Rimbau V (2003) C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4(3):207–216

    CAS  PubMed  Google Scholar 

  12. Osman MAH, Sheekh MM (2012) Hepatoprotective effect induced by NaCl stressed Spirulina platensis: histopathological, biochemical and histochemical studies. World Appl Sci J 18:1370–1380

    CAS  Google Scholar 

  13. Ivanova KG, Stankova KG, Nikolov VN, Georgieva RT, Minkova KM, Gigova LG, Rupova IT, Boteva RN (2010) The biliprotein C-phycocyanin modulates the early radiation response: a pilot study. Mutat Res 695(1–2):40–45

    CAS  PubMed  Google Scholar 

  14. Akimoto S, Yokono M, Hamada F, Teshigahara A, Aikawa S, Kondo A (2012) Adaptation of light-harvesting systems of Arthrospira platensis to light conditions, probed by time-resolved fluorescence spectroscopy. Biochimica et BiophysicaActa BBA Bioenergetics 1817:1483–1489

    CAS  Google Scholar 

  15. Kim NN, Shin HS, Park HG, Lee J, Kil GS, Choi CY (2014) Profiles of photosynthetic pigment accumulation and expression of photosynthesis-related genes in the marine cyanobacteria Synechococcus sp: Effects of LED wavelengths. Biotechnol Bioproc Eng 19:250–256

    CAS  Google Scholar 

  16. Chen HW, Yang TS, Chen MJ, Chang YC, Wang EIC, Ho CL, Lai YJ, Yu CC, Chou JC, Chao LKP, Liao PC (2014) Purification and immune modulating activity of C-phycocyanin from Spirulina platensis cultured using power plant flue gas. Process Biochem 49(8):1337–1344

    CAS  Google Scholar 

  17. Zarrouk C (1966) Contribution a l’etuded’unecyanobacterie: influence de divers facteurs physiques et chimiques sur la croissance et la photosynthese de Spirulina maxima (Setchell et Gardner) Geitler. PhD thesisUniversity of Paris, France

  18. Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89(1):27–41

    CAS  PubMed  Google Scholar 

  19. Lee HS, Castle WS (2001) Seasonal change of carotenoid pigments and color in Hamlin, Earlygold, and Budd Blood orange juices. J Agric Food Chem 49(2):877–882

    CAS  PubMed  Google Scholar 

  20. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  Google Scholar 

  21. Roe SH (1955) The determination of sugar in blood and spinal fluid with anthrone reagent. J Biol Chem 212(1):335–343

    CAS  PubMed  Google Scholar 

  22. Bennett A, Bogard L (1973) Complementary chromatic adaption in a filamentous blue-green alga. J Cell Biol 58(2):419–438

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Sobiechowska-Sasim M, Stoń-Egiert J, Kosakowska A (2014) Quantitative analysis of extracted phycobilin pigments in cyanobacteria—an assessment of spectrophotometric and spectrofluorometric methods. J Appl Phycol 26:2065–2074

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhang XF, Wang X, Luo GH (2017) Ultrasound-assisted three phase partitioning of phycocyanin from Spirulinaplatensis. Eur J Pure Appl Chem 4(1):1–15

    Google Scholar 

  25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    CAS  PubMed  Google Scholar 

  26. Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45(4):493–496

    CAS  PubMed  Google Scholar 

  27. Ruch RJ, Cheng SJ, Klaunig JE (1989) Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinog 10(6):1003–1008

    CAS  Google Scholar 

  28. Markou G, Georgakakis D (2011) Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. Appl Energy 88(10):3389–3401

    CAS  Google Scholar 

  29. Raeisossadati M, Moheimani NR, Parlevliet D (2019) Red and blue luminescent solar concentrators for increasing Arthrospira platensis biomass and phycocyanin productivity in outdoor raceway ponds. Bioresource Technol. https://doi.org/10.1016/j.biortech.2019.121801

    Article  Google Scholar 

  30. Costa JAV, Cozz KL, Oliveira L, Magagnin G (2001) Different nitrogen sources and growth responses of Spirulina platensis in microenvironments. World J Microbiol Biotechnol 17:439–442

    CAS  Google Scholar 

  31. Danesi EDG, Rangel-Yagui CO, Carvalho JCM, Sato S (2002) An investigation of the effect of replacing nitrate by urea in the growth and production of chlorophyll by Spirulina platensis. Biomass Bioenerg 23(4):261–269

    CAS  Google Scholar 

  32. Frede K, Schreiner M, Zrenner R, Graefe J, Baldermann S (2018) Carotenoid biosynthesis of pakchoi (Brassica rapa ssp. chinensis) sprouts grown under different light-emitting diodes during the diurnal course. Photochem Photobiol Sci 17(10):1289–1300

    CAS  PubMed  Google Scholar 

  33. Kitazaki C, Numano S, Takanezawa A, Nishizawa T, Shirai M, Asayama M (2013) Characterization of lysis of the multicellular cyanobacterium Limnothrix/Pseudanabaena sp. strain ABRG5–3. Biosci Biotechnol Biochem 77(12):2339–2347

    CAS  PubMed  Google Scholar 

  34. Walter A, Carvalho JC, Soccol VT, Faria ABB, Ghiggi V, Soccol CR (2011) Study of phycocyanin production from Spirulina platensis under different light spectra. Braz Arch BiolTechnol 54(4):675–682

    CAS  Google Scholar 

  35. Liu LN, Elmalk AT, Aartsma TJ, Thomas JC, Lamers GEM, Zhou BC, Zhang YZ (2008) Light-induced energetic decoupling as a mechanism for phycobilisome-related energy dissipation in red algae: a single-molecule study. PLoS ONE 3(9):e3134

    PubMed  PubMed Central  Google Scholar 

  36. Kuddus M, Singh P, Thomas G, Al-Hazimi A (2013) Recent developments in production and biotechnological applications of C-phycocyanin. BioMed Res Int. https://doi.org/10.1155/2013/742859

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rockwell NC, Martin SS, Lagarias JC (2016) Identification of cyanobacteriochromes detecting far-red light. Biochem 55(28):3907–3919. https://doi.org/10.1021/acs.biochem.6b00299

    Article  CAS  Google Scholar 

  38. Silva FS, Moraes CC, Kalil SJ (2018) C-phycocyanin purification: Multiple processes for different applications. Braz J Chem Eng 35(3):1117–1128

    Google Scholar 

  39. Kumar D, Dhar DW, Pabbi S, Kumar N, Walia S (2014) Extraction and purification of C-phycocyanin from Spirulina platensis (CCC540). Indian J Plant Physiol 19:184–188. https://doi.org/10.1007/s40502-014-0094-7

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lee RE (2008) Phycology, 4th edn. University Press, Cambridge

    Google Scholar 

  41. Vasantha T, Kumar A, Attri P, Venkatesu P, Devi RS (2014) The solubility and stability of amino acids in biocompatible ionic liquids. Protein Pept Lett 21(1):15–24

    CAS  PubMed  Google Scholar 

  42. Kannaujiya VK, Rastogi RP, Sinha RP (2014) GC constituents and relative codon expressed amino acid composition in cyanobacterial phycobiliproteins. Gene 546:162–171

    CAS  PubMed  Google Scholar 

  43. Calzadilla PI, Kirilovsky D (2020) Revisiting cyanobacterial state transitions. Photochem Photobiol Sci 19(5):585–603

    CAS  PubMed  Google Scholar 

  44. Patel A, Mishra S, Pawar R, Ghosh PK (2005) Purification and characterization of C-phycocyanin from cyanobacterial species of marine and freshwater habitat. Protein Expr Purif 40(2):248–255

    CAS  PubMed  Google Scholar 

  45. Sarada DVL, Kumar S, Rengasamy R (2011) Purified C-phycocyanin from Spirulina platensis (Nordstedt) geitler: a novel and potent agent against drug-resistant bacteria. World J Microbiol Biotechnol 27(4):779–783

    CAS  Google Scholar 

  46. Ozdemir G, Karabay NU, Dalay MC, Pazarbasi B (2004) Antibacterial activity of volatile component and various extracts of Spirulina platensis. Phytother Res 18:754–757

    CAS  PubMed  Google Scholar 

  47. Liu Q, Huang Y, Zhang R, Cai T, Cai Y (2016) Medicalapplicationof Spirulina platensis derived C-phycocyanin. Altern Med Evid Based Complement. https://doi.org/10.1155/2016/7803846

    Article  Google Scholar 

  48. El-Baky HHA, El-Baroty GS (2012) Characterization and bioactivity of phycocyanin isolated from Spirulina maxima grown under salt stress. Food Funct 3(4):381–388. https://doi.org/10.1039/c2fo10194g

    Article  CAS  Google Scholar 

  49. Chan DI, Prenner EJ, Vogel HJ (2006) Tryptophan-and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochimica et BiophysicaActa (BBA)-Biomembranes 1758(9):1184–1202

    CAS  Google Scholar 

  50. Niu JF, Wang GC, Lin XZ, Zhou BC (2007) Large-scale recovery of C-phycocyanin from Spirulina platensis using expanded bed adsorption chromatography. J Chromatogr B Anal Technol Biomed Life Sci 850(1–2):267–276

    CAS  Google Scholar 

  51. Colla LM, Furlong EB, Costa JAV (2007) Antioxidant Properties of Spirulina (Arthospira) platensis cultivated under different temperatures and nitrogen regimes. Braz Arch Biol Technol 50(1):161–167

    CAS  Google Scholar 

  52. Santiago-Morales IS, Trujillo-Valle L, Marquez-Rocha FJ, Hernández JFL (2018) Tocopherols, phycocyanin and superoxide dismutase from microalgae: as potential food antioxidants. Appl Food Biotechnol 5(1):19–27

    CAS  Google Scholar 

  53. Ercolano G, De Cicco P, Ianaro A (2019) New drugs from the sea: pro-apoptotic activity of sponges and algae derived compounds. Mar Drugs 17(1):E31. https://doi.org/10.3390/md17010031

    Article  CAS  PubMed  Google Scholar 

  54. Li B, Chu X, Gao M, Li W (2010) Apoptotic mechanism of MCF-7 breast cells in vivo and in vitro induced by photodynamic therapy with C-phycocyanin. Acta Biochim Biophys Sin (Shanghai) 42(1):80–89

    CAS  Google Scholar 

  55. Putri AK, Dimarti SC, Yuniati R, Susilaningsih N (2020) Cytotoxicity and antiproliferation of phycocyanin from spirulina platensis extract on WiDr colon cancer cell line. Biosaintifika: J Biol Biol Educ 12(1):42–49

    Google Scholar 

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Acknowledgements

The first author Dr. S.Sivasankari would like to thank the Department of Science and Technology, New Delhi, India, for the fund (IF 140666) to support the research work. The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP-2020/134), King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Department of Biology, Gandhigram Rural Institute-DU, Gandhigram, Dindigul, Tamil Nadu, 624302, India

    Sivaprakasam Sivasankari & David Ravindran

  2. Research Department of Botany, Jamal Mohamed College, Tiruchirappalli, Tamil Nadu, 620020, India

    Mani Vinoth

  3. Department of Ecotoxicology and Genetic Toxicology, Ross Lifescience Pvt., Ltd., Pune, Maharastra, 411026, India

    Kathirvelu Baskar

  4. Plant Production Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box. 2460, Riyadh, 11451, Saudi Arabia

    Abdulaziz A. Alqarawi & Elsayed Fathi Abd_Allah

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  1. Sivaprakasam Sivasankari
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Sivasankari, S., Vinoth, M., Ravindran, D. et al. Efficacy of red light for enhanced cell disruption and fluorescence intensity of phycocyanin. Bioprocess Biosyst Eng 44, 141–150 (2021). https://doi.org/10.1007/s00449-020-02430-5

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