A Review on the Production of Blue Food colorant: Phycocyanin

Document Type : Review paper

Authors

1 Department of Food Industry, Basir Institute of Higher Education, P. O. Code: 3441356611, Abyek, Qazvin, Iran.

2 Agricultural mechanisation and industrial development center, Ministry of Agriculture-Jahad, P. O. Code: 1593416111, Tehran, Iran.

Abstract

Using natural colors in the food and pharmaceutical industries is very important. Natural colorants obtained from animals, plants and microorganisms are a promising alternative to artificial food colors because synthetic colors have a negative effect on human health in the long term. Phycocyanin is used as a natural blue and water-soluble colorant instead of artificial blue food dyes, which, in addition to coloring food, have potential useful properties as antioxidants and anticancer agents and have received scientific and industrial attention. Phycocyanin is extracted from microalgae such as spirulina and has a health-giving role against various conditions such as cancer, anemia, inflammation, diabetes, obesity and neurological disorders. It has also gained popularity due to its various applications in various food and pharmaceutical industries. This research has discussed an overview of the biotechnological production of phycocyanin edible blue colorant from spirulina microalgae, microbial culture, extraction, purification, stability methods, and its applications.

Keywords

Main Subjects


Pourasad M, Akbari Adergani B, Baghaei H. Edible colors in the food industry, connections and attractiveness. 23rd National Congress of Food Science and Industry of Iran. 2014; Quchan [In Persion].
2. Bahremand M, Abayi A, Soleimani Rad A. Evaluation of the potential of using carotenoids and other natural pigments as food colorings. the first national conference on snacks. 2013; Mashhad [In Persion].
3. Mokhtarian M, Tavakoli Sh, Types of natural food colors produced by microorganisms and their application in food industry. 10th National Conference on Sustainable Agriculture and Natural Resources, 2019; Tehran [In Persion].
4. Ghamari M, Rezagholi Y. A review of the biotechnological production of edible colors. the 6th International Conference on Agricultural and Environmental Engineering with a sustainable development approach. 2019 [In Persion].
5. Shahbazi M, Fekrat F, Nami B, Ghaffari A, Extraction and purification of phycocyanin pigment from Spirulina microalgae. Agricultural Biotechnology Research Institute. 2018; (30) [In Persion].
6. Tanaka T, Takahashi O, Inomata A, Ogata A, Nakae D. Reproductive and neurobehavioral effects of brilliant blue FCF in mice. Birth Defects Res B Dev Reprod Toxicol. 2012;95(6):395-409. https://doi.org/10.1002/bdrb.21029.
7. Ashaolu TJ, Samborska K, Lee CC, Tomas M, Capanoglu E, Tarhan Ö, et al. Phycocyanin, a super functional ingredient from algae; properties, purification characterization, and applications. Int J Biol Macromol. 2021;193:2320-2331. https://doi.org/10.1016/j.ijbiomac. 2021.11.064. 
8. Olas B, Białecki J, Urbańska K, Bryś M. The effects of natural and synthetic blue dyes on human health: A review of current knowledge and therapeutic perspectives. Adv Nutr. 2021;12(6):2301-2311. https://doi.org/10.1093/advances/ nmab081.
9. Ramesh C, Vinithkumar NV, Kirubagaran R, Venil CK, Dufossé L. Multifaceted applications of microbial pigments: current knowledge, challenges and future directions for public health implications. Microorganisms. 2019;7(7):186. https://doi.org/10.3390/microorganisms7070186.
10. Ashharshanjani N, Sheikhinejad A, Hosseinpour N. Investigation of phycocyanin pigment extraction according to spirulina strain growth variables in different culture environments. 10th International Conference on Food Industry Science, Organic Agriculture and Food Security. 1401. https://civilica.com/doc/1489330 [In Persion].
11. Faraji D, Rezaei K, Golmakani MT, Hashemi Ravan M. Optimization of phycocyanin production from spirulina algae under different cultivation conditions, 20th National Congress of Food Science and Industry, 2018; Tehran. https://civilica.com/doc/148729 [In Persion].
12. Hsieh-Lo M, Castillo G, Ochoa-Becerra MA, Mojica L. Phycocyanin and phycoerythrin: Strategies to improve production yield and chemical stability. Algal Res. 2019;42:101600. https://doi.org/10.1016/j.algal.2019.101 600.
13. Rasmi Mamaghani H, vaghari H, Ahmadi O, Jafarizadeh Malmiri H. Phycocyanin pigment: its importance, application and extraction method. 6th International Conference on Food Industry Science, Organic Agriculture and Food Security. 2019 [In Persion].
14. Jiang L, Wang Y, Yin Q, Liu G, Liu H, Huang Y, et al. Phycocyanin: a potential drug for cancer treatment. J. Cancer. 2017;8(17):3416. https://doi.org/10.7150 %2Fjca.21058.
15. Eriksen NT. Production of phycocyanin—a pigment with applications in biology, biotechnology, foods and medicine. Appl Microbiol Biotechnol. 2008;80(1):1-14. https://doi.org/10.1007/s00253-008-1542-y.
16. Santiago-Santos MC, Ponce-Noyola T, Olvera-Ramı́rez R, Ortega-López J, Cañizares-Villanueva RO. Extraction and purification of phycocyanin from Calothrix sp. Process Biochem. 2004;39(12):2047-2052. https://doi.org/10.1016/ J procbio.2003.10.007.
17. Kaur S, Khattar JI, Singh Y, Singh DP, Ahluwalia AS. Extraction, purification and characterisation of phycocyanin from Anabaena fertilissima PUPCCC 410.5: as a natural and food grade stable pigment. J Appl Phycol. 2019;31(3):1685-1696. https://doi.org/10.1007/s10811-018-1722-9.
18. Moon M, Mishra SK, Kim CW, Suh WI, Park MS, Yang JW. Isolation and characterization of thermostable phycocyanin from Galdieria sulphuraria. Korean J Chem Eng. 2014;31(3):490-495. https:/doi.org/10.1007/s11814-013-0239-9.
19. Choi WY, Lee HY. Effect of ultrasonic extraction on production and structural changes of C-phycocyanin from marine Spirulina maxima. Int. J. Mol. Sci. 2018;19(1):220. https://doi.org/10.3390/ijms19010220.
20. Patel V, Berthold D, Puranik P, Gantar M. Screening of cyanobacteria and microalgae for their ability to synthesize silver nanoparticles with antibacterial activity. Biotechnol. Rep. 2015;5:112-119. https://doi.org/10.1016 /j.btre.2014.12.001.
21. Gantar M, Simović D, Djilas S, Gonzalez WW, Miksovska J. Isolation, characterization and antioxidative activity of C-phycocyanin from Limnothrix sp. strain 37-2-1. J Biotechnol. 2012;159(1-2):21-26. https://doi.org/10.1016/ j.jbiotec.2012.02.004.
22. Soni B, Kalavadia B, Trivedi U, Madamwar D. Extraction, purification and characterization of phycocyanin from Oscillatoria quadripunctulata—Isolated from the rocky shores of Bet-Dwarka, Gujarat, India. Process Biochem. 2006;41(9):2017-2023. https://doi.org/10.1016/j.procbio. 2006.04.018.
23. Cuellar‐Bermudez SP, Aguilar‐Hernandez I, Cardenas‐Chavez DL, Ornelas‐Soto N, Romero‐Ogawa MA, Parra‐Saldivar R. Extraction and purification of high‐value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb Biotechnol. 2015;8(2):190-209. https://doi.org/10.1111/1751-7915.12167.
24. Patel A, Mishra S, Pawar R, Ghosh P.K. Purification and characterization of C-Phycocyanin from cyanobacterial species of marine and freshwater habitat. Protein Expr. Purif. 2005;40(2):248-255. https://doi.org/ 10.1016/j.pep.2004.10.028.
25. Barsanti L, Coltelli P, Evangelista V, Frassanito AM, Passarelli V, Vesentini N, et al. Algal Toxins: Nature, Occurrence, Effect and Detection. Oddities and curiosities in the algal world. NATO Science for Peace and Security Series A: Chemistry and Biology. (pp. 353-391). Springer, Dordrecht; 2008. https://doi.org/10.1007/978-1-4020-8480-5_17.
26. Benchikh Y, Filali A, Rebai S. Modeling and optimizing the phycocyanins extraction from Arthrospira platensis (Spirulina) algae and preliminary supplementation assays in soft beverage as natural colorants and antioxidants. J. Food Process Preserv. 2021;45(2):e15170. https://doi. org/ 10.1111/jfpp.15170.
27. Sharma G, Kumar M, Ali MI, Jasuja ND. Effect of carbon content, salinity and pH on Spirulina platensis for phycocyanin, allophycocyanin and phycoerythrin accumulation. J Microb Biochem Technol. 2014;6(4):202-206. https://doi.org/10.4172/1948-5948.1000144.
28. Athiyappan KD, Routray W, Paramasivan B. Phycocyanin from Spirulina: A comprehensive review on cultivation, extraction, purification, and its application in food and allied industries. Food and Humanity. 2024;2:100235. https://doi.org/10.1016/j.foohum.2024.100235.
29. AlFadhly NK, Alhelfi N, Altemimi AB, Verma DK, Cacciola F. Tendencies affecting the growth and cultivation of genus Spirulina: An investigative review on current trends. Plants. 2022;11(22):3063. https://doi.org/ 10.3390/plants11223063.
30. Dineshkumar R, Narendran R, Sampathkumar P. Cultivation of Spirulina platensis in different selective media. INDIAN J. MAR. SCI. 2016; 45(12):1749-1754. 
31. Soni RA, Sudhakar K, Rana RS. Comparative study on the growth performance of Spirulina platensis on modifying culture media. Energy Rep. 2019;5:327-336. https://doi.org/10.1016/j.egyr.2019.02.009.
32. Sheykhi Nejad A, Lababpour A.M, Moazami N. Increasing Cyanobacteria Spirulina Production with Mixing and Chemical Composition of Culture Medium. Journal of Plant Research (Iranian Journal of Biology). 2015; 28(2): 344-353. https://dorl.net/dor/20.1001.1.23832592. 1394.28.2.12.9 [In Persion].
33. Rahim A, Çakir C, Ozturk M, Şahin B, Soulaimani A, Sibaoueih M, et al. Chemical characterization and nutritional value of Spirulina platensis cultivated in natural conditions of Chichaoua region (Morocco). S Afr J Bot. 2021;141:235-242. https://doi.org/10.1016/j.sajb. 2021.05.006.
34. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N. Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol. 2000;123(3):1047-1056. https://doi.org/ 10.1104/pp.123.3.1047.
35. Fernandes R, Campos J, Serra M, Fidalgo J, Almeida H, Casas A, et al. Exploring the Benefits of Phycocyanin: From Spirulina Cultivation to Its Widespread Applications. Pharmaceuticals. 2023;16(4):592. https://doi.org/10.3390/ ph16040592.
36. Soni RA, Sudhakar K, Rana RS. Comparative study on the growth performance of Spirulina platensis on modifying culture media. Energy Rep. 2019;5:327-336. https:// doi.org/10.1016/j.egyr.2019.02.009.
37. Çelekli A, Yavuzatmaca M, Bozkurt H. Modeling of biomass production by Spirulina platensis as function of phosphate concentrations and pH regimes. Bioresour Technol. 2009;100(14):3625-3629. https://doi.org/10.1016 /j.biortech.2009.02.055.
38. Ogbonda KH, Aminigo RE, Abu GO. Influence of temperature and pH on biomass production and protein biosynthesis in a putative Spirulina sp. Bioresour Technol. 2007;98(11):2207-2211. https://doi.org/10.1016/j.biortech. 2006.08.028.
39. Poza-Carrión C, Fernández-Valiente E, Piñas FF, Leganés F. Acclimation of photosynthetic pigments and photosynthesis of the cyanobacterium Nostoc sp. strain UAM206 to combined fluctuations of irradiance, pH, and inorganic carbon availability. J Plant Physiol. 2001;158(11):1455-1461. https://doi.org/10.1078/0176-1617-00555.
40. Abd El-Baky HH. Over Production of Phycocyanin Pigment in Blue Green Alga Spirulina sp. and lt's Inhibitory Effect on. J Med Sci. 2003;3(4):314-324. https://doi.org/10.3923/jms.2003.314.324.
41. Adjali A, Clarot I, Chen Z, Marchioni E, Boudier A. Physicochemical degradation of phycocyanin and means to improve its stability: A short review. J Pharm Anal. 2022;12(3):406-414. https://doi.org/10.1016/j.jpha.2021. 12.005.
42. Mishra SK, Shrivastav A, Mishra S. Effect of preservatives for food grade C-PC from Spirulina platensis. Process Biochem. 2008;43(4):339-345. https://doi.org/10.1016/ j.procbio.2007.12.012.
43. Saito T, Ishikura H, Hada Y, Fukui K, Kodera Y, Matsushim A, et al. Photostabilization of phycocyanin and anthocyanin in the presence of biopterin-α-glucoside from Spirulina platensis under ultraviolet ray. Dyes pigm. 2003;56(3):203-207. https://doi.org/10.1016/ S0143-7208(02)00163-8.
44. Antelo FS, Costa JA, Kalil SJ. Thermal degradation kinetics of the phycocyanin from Spirulina platensis. Biochem Eng J. 2008;41(1):43-47. https://doi.org/ 10.1016/j.bej.2008.03.012.
45. Faieta M, Neri L, Sacchetti G, Di Michele A, Pittia P. Role of saccharides on thermal stability of phycocyanin in aqueous solutions. Food Res Int. 2020;132:109093. https://doi.org/10.1016/j.foodres.2020.109093.
46. Braga ARC, Figueira FD, Silveira JT, Morais MG, Costa JA, Kalil SJ. Improvement of thermal stability of c‐phycocyanin by nanofiber and preservative agents. J Food Process Preserv. 2016;40(6):1264-1269. https://doi.org/ 10.1111/jfpp.12711.
47. Martelli G, Folli C, Visai L, Daglia M, Ferrari D. Thermal stability improvement of blue colorant C-Phycocyanin from Spirulina platensis for food industry applications. Process Biochem. 2014;49(1):154-159. https:// doi.org/10.1016/ j.procbio.2013.10.008.
48. Chaiklahan R, Chirasuwan N, Bunnag B. Stability of phycocyanin extracted from Spirulina sp.: Influence of temperature, pH and preservatives. Process Biochem. 2012;47(4):659-664. https://doi.org/10.1016/j.procbio. 2012. 01.010.
49. Kuddus M, Singh P, Thomas G, Al-Hazimi A. Recent developments in production and biotechnological applications of C-phycocyanin. Biomed Res Int. 2013. https://doi.org/10.1155/2013/742859.
50. Zarandi-Miandoab L, Pouryousef F, Razavi S F, Chaparzadeh N. Phycocyanin, as a cyanobacterial antioxidant: structure, function and applications. Plant Proc Function. 2022;0(1):1-22. http://dorl.net/dor/20.1001. 1.23222727.1401.0.1.1.5. [In Persion].
51. Jaeschke DP, Teixeira IR, Marczak LD, Mercali GD. Phycocyanin from Spirulina: A review of extraction methods and stability. Food Res Int. 2021;143:110314. https://doi.org/10.1016/j.foodres.2021.110314.
52. Chittapun S, Jonjaroen V, Khumrangsee K, Charoenrat T. C-phycocyanin extraction from two freshwater cyanobacteria by freeze thaw and pulsed electric field techniques to improve extraction efficiency and purity. Algal Res. 2020;46:101789. https://doi.org/10.1016/j. algal.2020.101789.
53. Sarada RM, Pillai MG, Ravishankar GA. Phycocyanin from Spirulina sp: influence of processing of biomass on phycocyanin yield, analysis of efficacy of extraction methods and stability studies on phycocyanin. Process biochem. 1999;34(8):795-801. https://doi.org/10.1016/S0 032 -9592(98)00153-8.
54. Abalde J, Betancourt L, Torres E, Cid A, Barwell C. Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus sp. IO9201. Plant Sci. 1998;136(1):109-120. https://doi.org/10.1016/S0168-9452(98)00113-7.
55. Rigi M, Zarifjo M, Review on phycocyanin extraction from spirulina algae. 6th international conference on modern research in agricultural Engineering, environment, and natural resources. 2022; Tehran [In Persion].
56. Singh NK, Parmar A, Madamwar D. Optimization of medium components for increased production of C-phycocyanin from Phormidium ceylanicum and its purification by single step process. BioresourTechnol. 2009;100(4):1663-1669. https://doi.org/10.1016/j.biortech. 2008.09.021.
57. García-López DA, Olguín EJ, González-Portela RE, Sánchez-Galván G, De Philippis R, Lovitt RW, et al. A novel two-phase bioprocess for the production of Arthrospira (Spirulina) maxima LJGR1 at pilot plant scale during different seasons and for phycocyanin induction under controlled conditions. Bioresour Technol. 2020;298:122548. https://doi.org/ 10.1016/j.biortech. 2019. 122548.
58. Figueira FDS, Moraes CC, Kalil SJ. C-phycocyanin purification: Multiple processes for different applications. Braz J Chem Eng. 2018;35(3):1117-1128. https://doi.org/ 10.1590/0104-6632.20180353s20170160.