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Is downstream ultrafiltration enough for production of food-grade phycocyanin from Arthrospira platensis?

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Abstract

Phycocyanin (PC), a natural blue pigment found in the cyanobacterium Arthrospira platensis, has anticancer, anti-inflammatory, and antioxidant properties. The purity of PC is the key factor for its application in the food, pharmaceutical and medical industries; however, the purification processes needed to achieve high purity can impact its bioactivity. This study evaluates whether microfiltration (MF) or ultrafiltration (UF) can be used to produce PC with food-grade purity. MF and UF following freeze-thaw extraction of PC from A. platensis biomass resulted in a low product purity, with other cellular constituents forming a cake on the membrane surface during the filtration process and preventing the concentration of PC. Phosphate buffer extraction resulted in more PC (65.5 mg g−1) with purity of 0.53. When the UF was followed by one step of diafiltration, purity was further enhanced to 0.76. However, the purification resulted in a 30% loss of antioxidant activity. This study demonstrates that phosphate buffer extraction followed by UF and one step of DF is suitable to produce food-grade PC from A. platensis, with the advantage of only requiring a single piece of equipment to perform the purification.

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References

  • Abalde J, Betancourt L, Torres E, Cid A, Barwell C (1998) Purification and characterization of phycocyanin from the marine cyanobacterium Synechococcus sp. IO9201. Plant Sci 136:109–120

    CAS  Google Scholar 

  • Antelo FS, Costa JAV, Kalil SJ (2008) Thermal degradation kinetics of the phycocyanin from Spirulina platensis. Biochem Eng J 41:43–47

    CAS  Google Scholar 

  • Baldasso C, Barros TC, Tessaro IC (2011) Concentration and purification of whey proteins by ultrafiltration. Desalination 278:381–386

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT - Food Sci Technol 28:25–30

  • Brião VB, Seguenka B, Zanon CD, Milani A (2017) Cake formation and the decreased performance of whey ultrafiltration. Acta Scientiarum Technol 39:517–524

    Google Scholar 

  • Cavalheiro PL, Machado AR, Ribeiro AC, Furlong EB, Soares LS (2013) Evalutation of antioxidant activity of different extracts from Spirulina LEB-18 (Avaliação da capacidade antioxidante de diferentes extratos de microalga Spirulina LEB -18) In: 53° Brazilian Congress of Chemistry. http://www.abq.org.br/cbq/2013/trabalhos/10/2730-16304

  • Chaiklahan R, Chirasuwan N, Loha V, Tia S, Bunnag B (2011) Separation and purification of phycocyanin from Spirulina sp. using a membrane process. Bioresour Technol 102:7159–7164

    CAS  PubMed  Google Scholar 

  • Chaiklahan R, Chirasuwan N, Loha V, Tia S, Bunnag B (2018) Stepwise extraction of high-value chemicals from Arthrospira (Spirulina) and an economic feasibility study. Biotechnol Rep 20:e00280

    Google Scholar 

  • Chen K-H, Wang SS-S, Show P-L, Lin G-T, Chang Y-K (2018) A rapid and efficient technique for direct extraction of C-phycocyanin from highly turbid Spirulina platensis algae using hydrophobic interaction chromatography in stirred fluidized bed. Biochem Eng J 140:47–56

    Google Scholar 

  • Chen K-H, Wang SS-S, Show P-L, Hsu S-L, Shang Y-K (2019) Rapid and efficient recovery of C-phycocyanin from highly turbid Spirulina platensis algae using stirred fluidized bed ion exchange chromatography. Sep Purif Technol 209:636–645

    CAS  Google Scholar 

  • Corbatón-Báguena MJ, Vela MCV, Álvarez-Blanco S, Lora-García J (2013) Analysis of two ultrafiltration fouling models and estimation of model parameters as a function of operational conditions. Transp Porous Media 99:391–411

    Google Scholar 

  • El-Baky HHA, El-Baroty GS (2012) Characterization and bioactivity of phycocyanin isolated from Spirulina maxima grown under salt stress. Food Funct 3:381–388

    Google Scholar 

  • Eriksen NT (2008) Production of phycocyanin - a pigment with applications in biology, biotechnology, foods and medicine. Appl Microbiol Biotechnol 80:1–14

    CAS  PubMed  Google Scholar 

  • Estrada JEP, Bescós PB, del Fresno AMV (2001) Antioxidant activity of different fractions of Spirulina platensis protean extract. IL Farmaco 56:497–500

  • Fekrat F, Nami B, Ghanavati H, Ghaffari A, Shahbazi M (2019) Optimization of chitosan/activated charcoal-based purification of Arthrospira platensis phycocyanin using response surface methodology. J Appl Phycol:1095–1105

  • Fernández-Rojas B, Hernández-Juárez J, Pedraza-Chaverri J (2014) Nutraceutical properties of phycocyanin. J Funct Foods 11:375–392

    Google Scholar 

  • Ferreira-Hermosillo A, Torres-Duran PV, Juarez-Oropeza MA (2010) Hepatoprotective effects of Spirulina maxima in patients with non-alcoholic fatty liver disease: a case series. J Med Case Rep 4:1–5

    Google Scholar 

  • Figueira FS, Gettens JG, Costa JAV, Morais MG, Moraes CC, Kalil SJ (2016) Production of nanofibers containing the bioactive compound C-phycocyanin. J Nanosci Nanotechnol 16:944–949

    CAS  Google Scholar 

  • Gantar M, Simovic D, Djilas S, Gonzalez WW, Miksovska J (2012) Isolation, characterization and antioxidative activity of C-phycocyanin from Limnothrix sp. strain 37-2-1. J Biotechnol 159:21–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta A, Sainis JK (2010) Isolation of C-phycocyanin from Synechococcus sp., (Anacystis nidulans BD1). J Appl Phycol 22:231–233

    CAS  Google Scholar 

  • Herrera A, Boussiba S, Napoleone V, Hohlberg A (1989) Recovery of C-phycocyanin from cyanobacterium Spirulina maxima. J Appl Phycol 1:325–331

    Google Scholar 

  • Ho CC, Zydney AL (2000) A combined pore blockage and cake filtration model for protein fouling during microfiltration. J Colloid Interface Sci 232:389–399

    CAS  PubMed  Google Scholar 

  • İlter I, Akyıl S, Demirel Z, Koç M, Conk-Dalay M, Kaymak-Ertekin F (2018) Optimization of phycocyanin extraction from Spirulina platensis using different techniques. J Food Compos Anal 70:78–88

    Google Scholar 

  • Izadi M, Fazilati M (2018) Extraction and purification of phycocyanin from Spirulina platensis and evaluating its antioxidant and anti- inflammatory activity. Asian J Green Chem 2:364–379

    CAS  Google Scholar 

  • Jaouen P, Lépine B, Rossignol N, Royer R, Quéméneur F (1999) Clarification and concentration with membrane technology of a phycocyanin solution extracted from Spirulina platensis. Biotechnol Tech 13:877–881

    CAS  Google Scholar 

  • Jerley AA, Prabu DM (2015) Purification, characterization and antioxidant properties of C-phycocyanin from Spirulina platensis. Scrutiny Int Res J Ag Plant Biotech Bio Prod 2:7–16

    Google Scholar 

  • Kamble SP, Gaikar RB, Padalia RB, Shinde KD (2013) Extraction and purification of C-phycocyanin from dry Spirulina powder and evaluating its antioxidant, anticoagulation and prevention of DNA damage activity. J Appl Pharm Sci 3:149–153

    Google Scholar 

  • Kannaujiya VK, Sinha RP (2016) An efficient method for the separation and purification of phycobiliproteins from a rice-field cyanobacterium Nostoc sp. strain HKAR-11. Chromatographia 79:335–343

    CAS  Google Scholar 

  • Kannaujiya VK, Sinha RP (2016a) Thermokinetic stability of phycocyanin and phycoerythrin in food-grade preservatives. J Appl Phycol 28:1063–1070

    CAS  Google Scholar 

  • Karasu K, Yoshikawa S, Ookawara S, Ogawa K, Kentish SE, Stevens GW (2010) A combined model for the prediction of the permeation flux during the cross-flow ultrafiltration of a whey suspension. J Membr Sci 361:71–77

    CAS  Google Scholar 

  • Kaur S, Khattar JIS, Singh Y, Singh DP, Ahluwalia AS (2019) Extraction, purification and characterisation of phycocyanin from Anabaena fertilissima PUPCCC 410.5: as a natural and food grade stable pigment. J Appl Phycol 31:1685–1696

    CAS  Google Scholar 

  • Kelly ST, Zydney AL (1997) Protein fouling during microfiltration: comparative behavior of different model proteins. Biotechnol Bioeng 55(1):91–100

  • Khazi MI, Demirel Z, Dalay MC (2018) Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. J Appl Phycol 30:1513–1523

    CAS  Google Scholar 

  • Krimm BS, Bandekart J (1986) Vibrational spectroscopy and conformation of peptides, polypeptides and proteins. Adv Protein Chem 38:181–364

    CAS  PubMed  Google Scholar 

  • Larossa APQ, Camara ÁS, Moura JM, Pinto LAA (2018) Spirulina sp. biomass dried/disrupted by different methods and their application in biofilms production. Food Sci Biotechnol 27:1659–1665. https://doi.org/10.1007/s10068-018-0397-y

  • Lee S-H, Lee JE, Kim Y, Lee S-Y (2016) The production of high purity phycocyanin by Spirulina platensis using light-emitting diodes based two-stage cultivation. Appl Biochem Biotechnol 178:382–395

    CAS  PubMed  Google Scholar 

  • Manirafasha E, Murwanashyaka T, Ndikubwimana T, Yue Q, Zeng X, Lu Y, Jing K (2017) Ammonium chloride: a novel effective and inexpensive salt solution for phycocyanin extraction from Arthrospira (Spirulina) platensis. J Appl Phycol 29:1261–1270

    CAS  Google Scholar 

  • Mensor LL, Menezes FS, Leitão GG, Reis AS, dos Santos TC, Coube CS, Leitão SG (2001) Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytoterapy Res 15:127–130

    CAS  Google Scholar 

  • Mogany T, Kumari S, Swalaha FM, Bux F (2019) Extraction and characterisation of analytical grade C-phycocyanin from Euhalothece sp. J Appl Phycol 31:1661–1675

    CAS  Google Scholar 

  • Moraes CC, Sala L, Cerveira GP, Kalil SJ (2011) C-phycocyanin extraction from Spirulina platensis wet biomass. Braz J Chem Eng 28:45–49

    CAS  Google Scholar 

  • Morais MG, Radmann EM, Andrade MR, Teixeira GG, Brusch LRF, Costa JAV (2009) Pilot scale semicontinuous production of Spirulina biomass in southern Brazil. Aquaculture 294:60–64

    Google Scholar 

  • Nourbakhsh H, Emam-Djomeh Z, Mirsaeedghazi H, Omid M, Moeni S (2014) Study of different fouling mechanisms during membrane clarification of red plum juice. Int J Food Sci Technol 49:58–64

    CAS  Google Scholar 

  • Pagno CH, Baldasso C, Tessaro IC, Flores SH, de Jong EV (2009) Obtenção de concentrados proteicos de soro de leite e caracterização de suas propriedades funcionais tecnológicas. Alimentos e Nutrição 20:231–239

    CAS  Google Scholar 

  • Paliwal C, Bhayani K, Gosh T, Bahyani K, Maurya R, Mishra S (2015) Antioxidant, anti-nephrolithe activities and in vitro digestibility studies of three different cyanobacterial pigment extracts. Mar Drugs 13:5384–5401

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 40:248–255

    CAS  PubMed  Google Scholar 

  • Patil G, Chethana S, Madhusudhan MC, Raghavarao KSMS (2008) Fractionation and purification of the phycobiliproteins from Spirulina platensis. Bioresour Technol 99:7393–7396

    CAS  PubMed  Google Scholar 

  • Peng H, Tremblay AY (2008) Membrane regeneration and filtration modeling in treating oily wastewaters. J Membr Sci 324:59–66

    CAS  Google Scholar 

  • Ramos A, Acién FG, Fernández-Sevilla JM, González CV, Bermejo R (2010) Large-scale isolation and purification of C-phycocyanin from the cyanobacteria Anabaena marina using expanded bed adsorption chromatography. J Chem Technol Biotechnol 85:783–792

    CAS  Google Scholar 

  • Raposo MFJ, Morais RMSC, Morais AMMB (2013) Health applications of bioactive compounds from marine microalgae. Life Sci 93:479–486

    CAS  Google Scholar 

  • Renugadevi K, Nachiyar CV, Sowmiya P, Sunkar S (2018) Biocatalysis and agricultural biotechnology antioxidant activity of phycocyanin pigment extracted from marine filamentous cyanobacteria Geitlerinema sp TRV57. Biocatal Ag Biotechnol 16:237–242

    Google Scholar 

  • Ruiz CAS, Emmery DP, Wijffels RH, Eppink MHM, van der Berg C (2018) Selective and mild fractionation of microalgal proteins and pigments using aqueous two-phase systems. J Chem Technol Biotechnol 93:2774–2783

    Google Scholar 

  • Sala L, Moraes CC, Kalil SJ (2018) Cell pretreatment with ethylenediaminetetraacetic acid for selective extraction of C-phycocyanin with food grade purity. Biotech Progr 34:1261–1268

    CAS  Google Scholar 

  • Sarada R, Pillai MG, Ravishankar GA (1999) 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 34:795–801

    CAS  Google Scholar 

  • Saran S, Puri N, Jasuja ND, Kumar M, Sharma G (2016) Optimization, purification and characterization of phycocyanin from Spirulina platensis. Int J Appl Pure Sci Ag 2:15–21

    Google Scholar 

  • Silveira ST, Burkert JFM, Costa JAV, Burkert CAV, Kalil SJ (2007) Optimization of phycocyanin extraction from Spirulina platensis using factorial design. Bioresour Technol 98:1629–1634

    CAS  PubMed  Google Scholar 

  • Sonani RR, Gupta GD, Madamwar D, Kumar V (2015) Crystal structure of allophycocyanin from marine cyanobacterium Phormidium sp. A09DM. PLoS One 10:e0124580

    PubMed  PubMed Central  Google Scholar 

  • Soni B, Trivedi U, Madamwar D (2008) A novel method of single step hydrophobic interaction chromatography for the purification of phycocyanin from Phormidium fragile and its characterization for antioxidant property. Bioresour Technol 99:188–194

    CAS  PubMed  Google Scholar 

  • Taniguchi M, Kilduff JE, Belfort G (2003) Modes of natural organic matter fouling during ultrafiltration. Environ Sci Technol 37:1676–1683

    CAS  PubMed  Google Scholar 

  • Tavanandi HA, Mittal R, Chandrasekhar J, Raghavarao KSMS (2018) Simple and efficient method for extraction of C-phycocyanin from dry biomass of Arthospira platensis. Algal Res 31:239–251

    Google Scholar 

  • Tavanandi HA, Devi AC, Raghavarao KSMS (2018a) A newer approach for the primary extraction of allophycocyanin with high purity and yield from dry biomass of Arthrospira platensis. Sep Purif Technol 204:162–174

    CAS  Google Scholar 

  • Tsakali E, Petrotos K, D’Alessandro AG, Mantas C, Tripolitsiotis GP, Chatzilazarou A, van Impe JF (2015) Exploring the effect of ultrafiltration/diafiltration processing conditions on the lactoferrin and immunoglobulin G content of feta whey protein concentrates. J Food Process Eng 38:363–373

    CAS  Google Scholar 

  • Vela MCV, Blanco SÁ, García JL, Rodríguez EB (2008) Fouling dynamics modelling in the ultrafiltration of PEGs. Desalination 222:451–456

    CAS  Google Scholar 

  • Xia D, Liu B, Xin W, Liu T, Sun J, Liu N, Qin S, Du Z (2016) Protective effects of C-phycocyanin on alcohol-induced subacute liver injury in mice. J Appl Phycol 28:765–772

    CAS  Google Scholar 

  • Yee KWK, Wiley DE, Bao J (2009) A unified model of the time dependence of flux decline for the long-term ultrafiltration of whey. J Membr Sci 332:69–80

    CAS  Google Scholar 

  • Zarrouk C (1966) Contribution l'étude d'une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthése de Spirulina maxima. Doctoral Thesis, University of Paris

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  1. School of Engineering, University of Passo Fundo, BR 285 Road, km 171, PO Box 611, Passo Fundo, Rio Grande do Sul State, 99052-900, Brazil

    Vandré Barbosa Brião, Alessandro Lima Sbeghen, Luciane Maria Colla, Vinicius Castoldi & Bruna Seguenka

  2. Federal University of Rio Grande do Sul, Porto Alegre, Brazil

    Guilherme de Oliveira Schimidt

  3. Federal University of Rio Grande, Rio Grande, Brazil

    Jorge Alberto Vieira Costa

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  1. Vandré Barbosa Brião
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  2. Alessandro Lima Sbeghen
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  3. Luciane Maria Colla
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  4. Vinicius Castoldi
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  5. Bruna Seguenka
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  6. Guilherme de Oliveira Schimidt
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  7. Jorge Alberto Vieira Costa
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Brião, V.B., Sbeghen, A.L., Colla, L.M. et al. Is downstream ultrafiltration enough for production of food-grade phycocyanin from Arthrospira platensis?. J Appl Phycol 32, 1129–1140 (2020). https://doi.org/10.1007/s10811-019-02006-1

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