Enhancing the production of phycocyanin biopigment from microalga Arthrospira maxima through medium manipulation utilizing Box-Behnken Design
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MUHAMMAD SYAWALUDDIN HILMI YAHYA
MURNI HALIM
https://orcid.org/0000-0002-5744-2147
FADZLIE WONG FAIZAL WONG
HELMI WASOH
https://orcid.org/0000-0003-1447-3610
JOO SHUN TAN
https://orcid.org/0000-0002-5074-2016
MOHD SHAMZI MOHAMED
♥
https://orcid.org/0000-0002-9813-2161
Abstract
Abstract. Yahya MSH, Halim M, Wong FWF, Wasoh H, Tan JS, Mohamed MS. 2024. Enhancing the production of phycocyanin biopigment from microalga Arthrospira maxima through medium manipulation utilizing Box Behnken Design. Nusantara Bioscience 16: 263-276. Phycocyanin is among the valuable pigments produced by microalgae Arthrospira spp. possessing significant nutritional and coloring properties. It is widely used in food, nutraceutical, and biotechnology applications. Presently, Arthrospira platensis is a species very much established for producing phycocyanin commercially. Given the extensive research works and understanding of A. platensis, there exists a significant opportunity to explore lesser-studied but potentially valuable strains, such as A. maxima, specifically for pigment production capabilities. This study aims to optimize the phycocyanin production from the A. maxima by first considering vital media components for phycocyanin secretion by the microalgal cells, namely sodium nitrate, sodium bicarbonate, dipotassium phosphate, sodium chloride and a number of precursors. Upon identifying the most significant factors, their composition in the NRC production medium was manipulated using Response Surface Methodology (RSM). Initial screening using the Plackett-Burman Design revealed two macronutrients and a precursor that significantly affected the target response (?>0.05): sodium nitrate, dipotassium phosphate and glutamic acid. The three factors were further refined using the Box-Behnken Design (BBD), a variation of the RSM technique. In one BBD run, the highest phycocyanin yield was 224.86 mg/L, achieved using a recipe comprising 0.0125 M sodium nitrate, 0.375 mM dipotassium phosphate and 0.625 mM L-glutamic acid. This resulted in an increase of 37.85% improvement over the basal medium. BBD's validating recipe comprising 0.0125 M sodium nitrate, 0.375 mM dipotassium phosphate and 0.625 mM L-glutamic acid then produced 235.98 g/L of phycocyanin, which in turn has a 44.67% improvement of phycocyanin yield compared with an unoptimized NRC medium. This significant increase in phycocyanin yield demonstrates the potential of this research to enhance phycocyanin production for commercial use and further research. In conclusion, optimizing the composition of a medium can significantly increase phycocyanin production.
2019-01-01
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References
Ait-Amir B, Pougnet P, El Hami A. 2020. 6 - Meta-Model Development. In: Pougnet E (eds.). Embedded Mechatronic Systems 2. ISTE. DOI: 10.1016/B978-1-78548-190-1.50006-2.
Akbarnezhad M, Mehrgan MS, Kamali A, Baboli MJ. 2020. Effects of microelements (Fe Cu Zn) on growth and pigment contents of Arthrospira (Spirulina) platensis. Iranian J Fisher Sci 19 (2): 653-668. DOI: 10.22092/ijfs.2019.120614.
AlFadhly NKZ, Alhelfi N, Altemimi AB, Verma DK, Cacciola F. 2022. Tendencies affecting the growth and cultivation of genus Spirulina: An investigative review on current trends. Plants 11 (22): 1-21. DOI: 10.3390/plants11223063.
Banayan S, Jahadi M, Khosravi-Darani K. 2022. Pigment productions by Spirulina platensis as a renewable resource. J Appl Biotechnol Rep 9 (2): 614-621. DOI: 10.30491/jabr.2021.292076.1406.
Benavente-Valdés JR, Aguilar C, Contreras-Esquivel JC, Méndez-Zavala A, Montañez J. 2016. Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10: 117-125. DOI: 10.1016/j.btre.2016.04.001.
de Castro GFPDS, Rizzo RF, Passos TS, dos Santos BNC, Dias DDS, Domingues JR, Araújo KGDL. 2015. Biomass production by Arthrospira platensis under different culture conditions. Food Sci Technol 35 (1): 18-24. DOI: 10.1590/1678-457X.6421.
Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldivar R. 2015. Extraction and purification of high-value metabolites from microalgae: Essential lipids, astaxanthin and phycobiliproteins. Microbial Biotechnol 8 (2): 190-209. DOI: 10.1111/1751-7915.12167.
Das AK, Dewanjee S. 2018. Optimization of extraction using mathematical models and computation. In: Sarker SD, Nahar L (eds). Computational Phytochemistry. Elsevier, Amsterdam. DOI: 10.1016/B978-0-12-812364-5.00003-1.
Fattore N, Bellan A, Pedroletti L, Vitulo N, Morosinotto T. 2021. Acclimation of photosynthesis and lipids biosynthesis to prolonged nitrogen and phosphorus limitation in Nannochloropsis gaditana. Algal Res 58: 102368. DOI: 10.1016/j.algal.2021.102368.
Fekrat F, Shahbazi M, Nami B, Amin Hejazi M, Ghaffari MR. 2021. Nitrogen-containing metabolic stressors stimulate high-value compounds accumulation in Arthrospira platensis. Authorea DOI: 10.22541/au.161555554.40888746/v1.
Fleurence J, Levine IA. 2018. Antiallergic and allergic properties. In: Levine IA, Fleurence (eds). Microalgae in Health and Disease Prevention. Academic Press, London. DOI: 10.1016/B978-0-12-811405-6.00014-1.
Fujisawa T, Narikawa R, Okamoto S et al. 2010. Genomic structure of an economically important cyanobacterium, Arthrospira (Spirulina) platensis NIES-39. DNA Res 17 (2): 85-103. DOI: 10.1093/dnares/dsq004.
Furmaniak MA, Misztak AE, Franczuk MD, Wilmotte A, Waleron M, Waleron KF. 2017. Edible cyanobacterial genus Arthrospira: Actual state of the art in cultivation methods, genetics, and application in medicine. Front Microbiol 8: 02541. DOI: 10.3389/fmicb.2017.02541.
Gujral G, Kapoor D, Jaimini M. 2018. An updated review on Design of Experiment (Doe) in pharmaceuticals. J Drug Deliv Ther 8 (3): 147-152. DOI: 10.22270/jddt.v8i3.1713.
Hao C, Bing-jie Y, Tao L, Hua-lian W, Hou-bo W, Wen-zhou X. 2019. Effects of phosphorus concentrations on growth and metabolism of seawater Spirulina platensis. Biotechnol Bull 35 (8): 103-110. DOI: 10.13560/j.cnki.biotech.bull.1985.2019-0181.
Jankovic A, Chaudhary G, Goia F. 2021. Designing the Design of Experiments (DOE) – An investigation on the influence of different factorial designs on the characterization of complex systems. Energy Build 250: 111298. DOI: 10.1016/j.enbuild.2021.111298.
Kotinskyi AV, Zhadan S, Salyuk AI. 2018. The influence of exogenous glycine on growth and intensity of cyanobacteria Spirulina ?latensis (Gom.) Geitl photosynthetic processes. Biotechnol Acta 11 (6): 39-46. DOI: 10.15407/biotech11.06.039.
Kumar A, Bera S. 2020. Revisiting nitrogen utilization in algae: A review on the process of regulation and assimilation. Bioresour Technol Rep 12: 100584.
Lee BCY, Mahtab MS, Neo TH, Farooqi IH, Khursheed A. 2022. A comprehensive review of Design of Experiment (DOE) for water and wastewater treatment application - Key concepts, methodology and contextualized application. J Water Process Eng 47: 102673. DOI: 10.1016/j.jwpe.2022.102673.
Liotenberg S, Campbell D, Rippka R, Houmard J, Tandeau De Marsac N. 1996. Effect of the nitrogen source on phycobiliprotein synthesis and cell reserves in a chromatically adapting filamentous Cyanobacterium. Microbiology 142 (3): 611-622. DOI: 10.1099/13500872-142-3-611.
Magwell PFR, Djoudjeu KT, Minyaka E, Tavea MF, Fotsop OW, Tagnikeu RF, Fofou AM, Darelle CKV, Dzoyem CUD, Lehman LG. 2023. Sodium bicarbonate (NaHCO3) increases growth, protein and photosynthetic pigments production and alters carbohydrate production of Spirulina platensis. Curr Microbiol 80 (2): 63. DOI: 10.1007/s00284-022-03165-0.
Manirafasha E, Murwanashyaka T, Ndikubwimana T, Rashid Ahmed N, Liu J, Lu Y, Zeng X, Ling X, Jing K. 2018. Enhancement of cell growth and phycocyanin production in Arthrospira (Spirulina) platensis by metabolic stress and nitrate fed-batch. Bioresour Technol 255: 293-301. DOI: 10.1016/j.biortech.2017.12.068.
Manirafasha E, Ndikubwimana T, Zeng X, Lu Y, Jing K. 2016. Phycobiliprotein: Potential microalgae derived pharmaceutical and biological reagent. Biochem Eng J 109: 282-296. DOI: 10.1016/j.bej.2016.01.025.
Markou G, Chatzipavlidis I, Georgakakis D. 2012a. Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: Improvements through phosphorus limitation process. Bioenergy Res 5 (4): 915-925. DOI: 10.1007/s12155-012-9205-3.
Markou G, Chatzipavlidis I, Georgakakis D. 2012b. Effects of phosphorus concentration and light intensity on the biomass composition of Arthrospira (Spirulina) platensis. World J Microbiol Biotechnol 28 (8): 2661-2670. DOI: 10.1007/s11274-012-1076-4.
Markou G, Kougia E, Arapoglou D, Chentir I, Andreou V, Tzovenis I. 2023. Production of Arthrospira platensis: Effects on growth and biochemical composition of long-term acclimatization at different salinities. Bioengineering 10 (2): 233. DOI: 10.3390/bioengineering10020233.
Markou G, Vandamme D, Muylaert K. 2014. Microalgal and cyanobacterial cultivation: The supply of nutrients. Water Res 65: 186-202. DOI: 10.1016/j.watres.2014.07.025.
Mirhosseini N, Davarnejad R, Hallajisani A, Cano-Europa E, Tavakoli O. 2022. Sugarcane molasses as a cost-effective carbon Source on Arthrospira maxima growth by Taguchi technique. Intl J Eng 35 (3): 510-516. DOI: 10.5829/IJE.2022.35.03C.03.
Mirhosseini N, Davarnejad R, Hallajisani A, Cano-Europa E, Tavakoli O, Franco-Colín M, Blas-Valdivia V. 2021. Cultivations of Arthrospira maxima (Spirulina) using ammonium sulfate and sodium nitrate as an alternative nitrogen sources. Iran J Fish Sci 20 (2): 475-489. DOI: 10.22092/ijfs.2021.351071.0.
Moheimani NR, Borowitzka MA, Isdepsky A, Sing SF. 2013. Standard methods for measuring growth of algae and their composition. In: Borowitzka MA, Moheimani NR (eds). Algae for Biofuels and Energy. Springer, Dordrecht. DOI: 10.1007/978-94-007-5479-9_16.
Moraes CC, Sala L, Cerveira GP, Kalil SJ. 2011. C-Phycocyanin extraction from Spirulina platensis wet biomass. Braz J Chem Eng 28 (1): 45-49. DOI: 10.1590/S0104-66322011000100006.
Musifa E, Kusnanda AJ, Dharma A, Armaini. 2023. Monosodium Glutamate (MSG) as metabolic stressors stimulate the production of valuable compounds in Spirulina platensis. Egypt J Aquat Biol Fish 27 (2): 731-743. DOI: 10.21608/ejabf.2023.297611.
Nur MMA, Garcia GM, Boelen P, Buma AGJ. 2019. Enhancement of C-phycocyanin productivity by Arthrospira platensis when growing on palm oil mill effluent in a two-stage semi-continuous cultivation mode. J Appl Phycol 31 (5): 2855-2867. DOI: 10.1007/s10811-019-01806-9.
Pagels F, Guedes AC, Amaro HM, Kijjoa A, Vasconcelos V. 2019. Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications. Biotechnol Adv 37 (3): 422-443. DOI: 10.1016/j.biotechadv.2019.02.010.
Ragusa I, Nardone GN, Zanatta S, Bertin W, Amadio E. 2021. Spirulina for skin care: A bright blue future. Cosmetics 8 (1): 7. DOI: 10.3390/cosmetics8010007.
Roda-serrat MC, Christensen KV, El-houri RB, Fretté X, Christensen LP. 2018. Fast cleavage of phycocyanobilin from phycocyanin for use in food colouring. Food Chem 240: 655-661. DOI: 10.1016/j.foodchem.2017.07.149.
Senatore V, Rueda E, Bellver M, Díez-Montero R, Ferrer I, Zarra T, Naddeo V, García J. 2023. Production of phycobiliproteins, bioplastics and lipids by the cyanobacteria Synechocystis sp. treating secondary effluent in a biorefinery approach. Sci Total Environ 857: 159343. DOI: 10.1016/j.scitotenv.2022.159343.
Shanthi G, Premalatha M, Anantharaman N. 2018. Effects of L-amino acids as organic nitrogen source on the growth rate, biochemical composition and polyphenol content of Spirulina platensis. Algal Res 35: 471-478. DOI: 10.1016/j.algal.2018.09.014.
Stadnichuk IN, Tropin IV. 2017. Phycobiliproteins: Structure, functions and biotechnological applications. Appl Biochem Microbiol 53 (1): 1-10. DOI: 10.1134/S0003683817010185.
Thevarajah B, Nishshanka GKSH, Premaratne M, Nimarshana PHV, Nagarajan D, Chang JS, Ariyadasa TU. 2022. Large-scale production of Spirulina-based proteins and c-phycocyanin: A biorefinery approach. Biochem Eng J 185: 108541. DOI: 10.1016/j.bej.2022.108541.
Zarrouk C. 1966. Contribution a l’etude d’une Cyanophycee. Influence de Divers Facteurs Physiques et Chimiques sur la croissance et la photosynthese de Spirulina mixima. [Thesis]. University of Paris, Paris, France.
Zhou T, Wang J, Zheng H, Wu X, Wang Y, Liu M, Xiang S, Cao L, Ruan R, Liu Y. 2018. Characterization of additional zinc ions on the growth, biochemical composition and photosynthetic performance from Spirulina platensis. Bioresour Technol 269: 285-291. DOI: 10.1016/j.biortech.2018.08.131.