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Biomass and phycobiliprotein production of Galdieria sulphuraria, immobilized on a twin-layer porous substrate photobioreactor

  • Applied microbial and cell physiology
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Abstract

The extremophile red alga Galdieria sulphuraria was successfully grown immobilized in a twin-layer porous substrate bioreactor (TL-PSBR). A maximal biomass growth rate of 10 g dry weight m−2 day−1 was measured at a photon fluence rate of 200 μmol photons m−2 s−1 with addition of 1% CO2 and a temperature of 34 °C. Under these conditions, a maximal biomass value of 232 g m−2 was attained after 33 days of growth. Phycobilin productivity, however, was highest at a lower photon fluence rate of 100 μmol photons m−2 s−1 and reached a phycobilin value of 14 g m−2, a phycobilin content in the biomass of 63 mg g−1 and a phycobilin growth rate of 0.28 g m−2 day−1 for phycocyanin and 0.23 g m−2 day−1 for allophycocyanin. Addition of CO2 was essential to enhance growth and phycobilin production in G. sulphuraria and further optimization of the cultivation process in the TL-PSBR appears possible using a multi-phase approach, higher growth temperatures and optimization of nutrient supply. It is concluded that autotrophic cultivation of G. sulphuraria in a TL-PSBR is an attractive alternative to suspension cultivation for phycobilin production and applications in bioremediation.

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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 

  • Albertano P, Ciniglia C, Pinto G, Pollio A (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433:137–143

    Google Scholar 

  • Benstein RM, Cebi Z, Podola B, Melkonian M (2014) Immobilized growth of the peridinin-producing marine dinoflagellate Symbiodinium in a simple biofilm photobioreactor. Mar Biotechnol 16:621–628

    CAS  PubMed  Google Scholar 

  • Carbone DA, Olivieri G, Pollio A, Pinto G, Melkonian M (2017a) Growth and biomass productivity of Scenedesmus vacuolatus on a twin layer system and a comparison with other types of cultivations. Appl Microbiol Biotechnol 101:8321–8329

    CAS  PubMed  Google Scholar 

  • Carbone DA, Gargano I, Pinto G, De Natale A, Pollio A (2017b) Evaluating microalgal attachment to surfaces: a first approach towards a laboratory integrated assessment. Chem Eng Trans 57:73–78

    Google Scholar 

  • Carbone DA, Gargano I, Chiaiese P, Pollio A, Marotta R, Olivieri G, Pinto G (2018) Scenedesmus vacuolatus cultures for possible combined laccase-like phenoloxidase activity and biodiesel production. Ann Microbiol 68:9–15

    CAS  Google Scholar 

  • Carbone DA, Gargano I, Olivieri G, Marzocchella A, Andreozzi R, Marotta R, Spasiano D, Pinto G, Pollio A (2019) Light intensities maximizing photosynthesis and kinetics of photochemical steps in Graesiella emersonii under different cultivation strategies. Environ Eng Manag J 18:1527–1534

    Google Scholar 

  • Carfagna S, Salbitani G, Bottone C, Vona V (2016) Galdieria sulphuraria as a possible source of food colorant. J Nutr Ecol Food Res 3:78–81

    Google Scholar 

  • Carfagna S, Landi V, Coraggio F, Salbitani G, Vona V, Pinto G, Pollio A, Ciniglia C (2018) Different characteristics of C-phycocyanin (C-PC) in two strains of the extremophilic Galdieria phlegraea. Algal Res 31:46–52

    Google Scholar 

  • Castenholz RW, McDermott TR (2010) The Cyanidiales: ecology, biodiversity, and biogeography. In: Seckbach J, Chapman DJ (eds) Red Algae in the Genomic Age. Springer, Dordrecht, The Netherlands, pp 357–371

    Google Scholar 

  • Cennamo P, Marzano C, Ciniglia C, Pinto G, Cappelletti P, Caputo P, Pollio A (2012) A survey of the algal flora of anthropogenic caves of Campi Flegrei (Naples, Italy) archeological district. J Cave Karst Stud 74:243–250

    Google Scholar 

  • Centella MH, Arevalo-Gallegos A, Parra-Saldivar R, Iqbal HM (2017) Marine-derived bioactive compounds for value-added applications in bio-and non-bio sectors. J Clean Prod 168:1559–1565

    CAS  Google Scholar 

  • Chen F, Zhang Y (1997) High cell density mixotrophic culture of Spirulina platensis on glucose for phycocyanin production using a fed-batch system. Enzym Microb Technol 20:221–224

    CAS  Google Scholar 

  • Chen X, Wu M, Yang Q, Wang S (2017) Preparation, characterization of food grade phycobiliproteins from Porphyra haitanensis and the application in liposome-meat system. LWT Food Sci Technol 77:468–474

    CAS  Google Scholar 

  • Ciniglia C, Yoon HS, Pollio A, Pinto G, Bhattacharya D (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol Ecol 13:1827–1838

    CAS  PubMed  Google Scholar 

  • Ciniglia C, Yang EC, Pinto G, Iovinella M, Vitale L, Yoon HS (2014) Cyanidiophyceae in Iceland: plastid rbcL gene elucidates origin and dispersal of extremophilic Galdieria sulphuraria and Galdieria maxima (Galdieriaceae, Rhodophyta). Phycologia 53:542–551

    CAS  Google Scholar 

  • Ciniglia C, Iovinella M, Olivieri G, Cennamo P, Pollio A (2017) A potential use of the polyextremophilic microalga Galdieria sulphuraria (Cyanidiophyceae, Rodhophyta) in bio-recovery of rare metals. Phycologia Suppl 56:33

    Google Scholar 

  • Coward T, Fuentes-Grünewald C, Silkina A, Oatley-Radcliffe DL, Llewellyn G, Lovitt RW (2016) Utilising light-emitting diodes of specific narrow wavelengths for the optimization and co-production of multiple high-value compounds in Porphyridium purpureum. Bioresour Technol 221:607–615

    CAS  PubMed  Google Scholar 

  • Cozzolino S, Caputo P, De Castro O, Moretti A, Pinto G (2000) Molecular variation in Galdieria sulphuraria (Galdieri) Merola and its bearing on taxonomy. Hydrobiologia 433:145–151

    CAS  Google Scholar 

  • Dejsungkranont M, ChistiSarote Y, Sirisansaneeyakul S (2017) Optimization of production of C-phycocyanin and extracellular polymeric substances by Arthrospira sp. Bioprocess Biosyst Eng 40:1173–1188

    CAS  PubMed  Google Scholar 

  • Del Mondo A, Iovinella M, Petriccione A, Seth D, Cioppa D, Ciniglia C (2019) A spotlight on Rad52 in Cyanidiophytina (Rhodophyta): a relic in algal heritage. Plants 8(2):46

    PubMed Central  Google Scholar 

  • Do T, Ong B, Nguyen T, Melkonian M, Tran H (2019) Biomass and astaxanthin productivities of Haematococcus pluvialis in an angled twin-layer porous substrate photobioreactor: effect of inoculum density and storage time. Biology 8:68

    PubMed Central  Google Scholar 

  • Ekelhof A, Melkonian M (2017) Enhanced extracellular polysaccharide production and growth by microalga Netrium digitus in a porous substrate bioreactor. Algal Res 28:184–191

    Google Scholar 

  • Eren A, Iovinella M, Yoon HS, Cennamo P, de Stefano M, de Castro O, Ciniglia C (2018) Genetic structure of Galdieria populations from Iceland. Polar Biol 41:1681–1691

    Google Scholar 

  • Eriksen NT (2007) Production of phycocyanin — a pigment with applications in biology, biotechnology, foods and medicine. Appl Microbiol Biotechnol 80:1–14

    Google Scholar 

  • Eriksen NT (2013) Pigments from microalgae: a new perspective with emphasis on phycocyanin. In: Arlorio M (ed) Book of Abstracts and Proceedings of the 7th International Congress on Pigments in Foods. Aalborg University, Denmark, pp 37

  • Eriksen NT (2018) Heterotrophic production of phycocyanin in Galdieria sulphuraria. In: Durvasula RV, Subba Rao DV (eds) Extremophiles –from Biology to Biotechnology. CRC Press, Boca Raton, pp 87–101

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • da Fontoura PD, Radmann EM, Duarte JH, de Morais MG, Costa JAV (2018) Spirulina cultivated under different light emitting diodes: enhanced cell growth and phycocyanin production. Bioresour Technol 256:38–43

    Google Scholar 

  • Fukuda SYA, Yamamoto R, Iwamoto K, Minoda A (2018) Cellular accumulation of caesium in the unicellular red alga Galdieria sulphuraria under mixotrophic conditions. J Appl Phycol 30:3057–3061

    CAS  Google Scholar 

  • Gantt E (1980) Structure and function of phycobilisomes: light-harvesting pigment complexes in red and blue-green algae. Int Rev Cytol 56:45–80

    Google Scholar 

  • Gargano I, Olivieri G, Andreozzi R, Marotta R, Marzocchella A, Pollio A (2016) Biodiesel production in outdoor cultures of Scenedesmus vacuolatus. Chem Eng Trans 49:397–402

    Google Scholar 

  • Glazer AN (1994) Phycobiliproteins – a family of valuable, widely used fluorophores. J Appl Phycol 6:105–112

    CAS  Google Scholar 

  • Gordillo FL, Jimenez C, Figueroa FL, Niell FX (1998) Effects of increased atmospheric CO2 and N supply on photosynthesis, growth and cell composition of the cyanobacterium Spirulina platensis (Arthrospira). J Appl Phycol 10:461–469

    Google Scholar 

  • Graverholt OS, Eriksen NT (2007) Heterotrophic high cell-density fed-batch and continuous flow cultures of Galdieria sulphuraria and production of phycocyanin. Appl Microbiol Biotechnol 77:69–75

    CAS  PubMed  Google Scholar 

  • Graziani G, Schiavo S, Nicolai MA, Buono S, Fogliano V, Pinto G, Pollio A (2013) Microalgae as human food: chemical and nutritional characteristics of the thermo-acidophilic microalga Galdieria sulphuraria. Food Funct 4:144–152

    CAS  PubMed  Google Scholar 

  • Gross W (1999) Revision of comparative traits for the acid- and thermophilic red algae Cyanidium and Galdieria. In: Seckbach J (ed) Enigmatic Micro-organisms and Life in Extreme Environments. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 437–446

    Google Scholar 

  • Gross W, Schnarrenberger C (1995) Heterotrophic growth of two strains of the acid-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36:4–9

    Google Scholar 

  • Gross W, Kuver J, Tischendorf G, Bouchaala N, Busch W (1998) Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur J Phycol 33:25–31

    Google Scholar 

  • Grossman A, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisomes, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henkanatte-Gedera SM, Selvaratnam T, Karbakhshravari M, Myint M, Nirmalakhandan N, Van Voorhies W, Lammers PJ (2017) Removal of dissolved organic carbon and nutrients from urban wastewaters by Galdieria sulphuraria: laboratory to field scale demonstration. Algal Res 24:450–456

    Google Scholar 

  • Hirooka S, Miyagishima SY (2016) Cultivation of acidophilic algae Galdieria sulphuraria and Pseudochlorella sp. YKT1 in media derived from acidic hot springs. Front Microbiol 7:20–22

    Google Scholar 

  • Ho SH, Liao JF, Chen CY, Chang JS (2018) Combining light strategies with recycled medium to enhance the economic feasibility of phycocyanin production with Spirulina platensis. Bioresour Technol 247:669–675

    CAS  PubMed  Google Scholar 

  • Hsieh-Lo M, Castillo G, Ochoa-Becerra M, Mojica L (2019) Phycocyanin and phycoerythrin: strategies to improve production yield and chemical stability. Algal Res 42:50–56

    Google Scholar 

  • Imbimbo P, Romanucci V, Pollio A, Fontanarosa C, Amoresano A, Zarrelli A, Olivieri G, Monti DM (2019) A cascade extraction of active phycocyanin and fatty acids from Galdieria phlegraea. Appl Microbiol Biotechnol 103:9455–9464

    CAS  PubMed  Google Scholar 

  • Iovinella M, Eren A, Pinto G, Pollio A, Davis SJ, Cennamo P, Ciniglia C (2018) Cryptic dispersal in non-acidic environments from Turkey of Cyanidiophytina (Rhodophyta). Extremophile 22:713–723

    CAS  Google Scholar 

  • Jalali F, Fakhar J, Zolfaghari A (2019) Investigation on biosorption of V (III), Ti (IV), and U(VI) ions from a contaminated effluent by a newly isolated strain of Galdieria sulphuraria. Separat Sci Technol (Philadelphia) 54:914

    Google Scholar 

  • Ju X, Igarashi K, Miyashita K, Mitsuhashi H, Inagaki K, Fujii S, Sawada H, Kuwabara T, Minoda A (2016) Effective and selective recovery of gold and palladium ions from metal wastewater using a sulphothermophilic red alga, Galdieria sulphuraria. Bioresour Technol 211:759–764

    CAS  PubMed  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 

  • Kiperstok AC, Sebestyén P, Podola B, Melkonian M (2017) Biofilm cultivation of Haematococcus pluvialis enables a highly productive one-phase process for astaxanthin production using high light intensities. Algal Res 21:213–222

    Google Scholar 

  • Kuddus M, Singh P, Thomas G, Al-Hazimi A (2013) Recent developments in production and biotechnological applications of C-phycocyanin. Biomed Res Int 74:28–59

    Google Scholar 

  • Langenbach D, Melkonian M (2019) Optimising biomass and peridinin accumulation in the dinoflagellate Symbiodinium voratum using a twin-layer porous substrate bioreactor. J Appl Phycol 31:21–28

    CAS  Google Scholar 

  • Li T, Lin G, Podola B, Melkonian M (2015) Continuous removal of zinc from wastewater and mine dump leachate by a microalgal biofilm PSBR. J Hazard Mater 297:112–118

    CAS  PubMed  Google Scholar 

  • Li T, Piltz B, Podola B, Dron A, De Beer D, Melkonian M (2016) Microscale profiling of photosynthesis-related variables in a highly productive biofilm photobioreactor. Biotechnol Bioeng 113:1046–1055

    CAS  PubMed  Google Scholar 

  • Li T, Strous M, Melkonian M (2017) Biofilm-based photobioreactors: their design and improving productivity through efficient supply of dissolved inorganic carbon. FEMS Microbiol Lett 5:364–365

    Google Scholar 

  • Li W, Su H, Yang P, Chen J, Liu N, Liu Q, Qin S (2019) Phycobiliproteins: molecular structure, production, applications, and prospects. Biotechnol Adv 37:340–353

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Melkonian M, Podola B (2010) Method and device for cultivating eukaryotic microorganisms or blue algae, and biosensor with cultivated eukaryotic microorganisms or blue algae. United States Patent No US 7:745, 20

  • Minoda A, Sawada H, Suzuki S, Miyashita S, Inagaki K, Yamamoto T, Tsuzuki M (2015) Recovery of rare earth elements from the sulpho-thermophilic red alga Galdieria sulphuraria using aqueous acid. Appl Microbiol Biotechnol 99:1513–1519

    CAS  PubMed  Google Scholar 

  • Moon M, Mishra S, Kim C, Suh W, Park M, Yang J (2014) Isolation and characterization of thermostable phycocyanin from Galdieria sulphuraria. Korean J Chem Eng 31:490–495

    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 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    PubMed  PubMed Central  Google Scholar 

  • Naumann T, Çebi Z, Podola B, Melkonian M (2013) Growing microalgae as aquaculture feeds on twin-layers: a novel solid-state photobioreactor. J Appl Phycol 25:1413–1420

    CAS  Google Scholar 

  • Nowack E, Podola B, Melkonian M (2005) The 96-well twin-layer system: a novel approach in the cultivation of microalgae. Protist 156:239–251

    PubMed  Google Scholar 

  • Nwoba E, Parleveit A, Laird D, Kamal A, Moheiman E (2019) Light management technologies for increasing algal photobioreactor efficiency. Algal Res 39:18–21

    Google Scholar 

  • Olivieri G, Salatino P, Marzocchella A (2014) Advances in photobioreactors for intensive microalgal production: configurations, operating strategies and applications. J Chem Technol Biotechnol 89:178–195

    CAS  Google Scholar 

  • Osorio JHM, Pinto G, Pollio A, Frunzo L, Nicolaas P, Lens L, Esposito G (2019) Start-up of a nutrient removal system using Scenedesmus vacuolatus and Chlorella vulgaris biofilms. Biores Bioproc 6:27–29

    Google Scholar 

  • Pagels F, Guedes AC, Amaro H, Kijjoa H, Vasconcelos V (2019) Phycobiliproteins from cyanobacteria: chemistry and biotechnological applications. Biotechnol Adv 37:422–443

    CAS  PubMed  Google Scholar 

  • Pan-Utai W, Kahapana W, Iam S (2018) Extraction of C-phycocyanin from Arthrospira (Spirulina) and its thermal stability with citric acid. J Appl Phycol 30:231–242

    CAS  Google Scholar 

  • Pierobon SC, Cheng X, Graham PJ, Nguyen B, Karakolis EG, Sinton D (2018) Emerging microalgae technology: a review. Sustain Energy Fuels 2:13–38

    CAS  Google Scholar 

  • Piltz B, Melkonian M (2018) Immobilized microalgae for nutrient recovery from source-separated human urine. J Appl Phycol 30:421–429

    CAS  Google Scholar 

  • Pinto G (2007) Cyanidiophyceae: looking back—looking forward. In: Seckbach J (ed) Algae and Cyanobacteria in Extreme Environments. Springer, Dordrecht, The Netherlands, pp 389–397

    Google Scholar 

  • Pinto G, Ciniglia C, Cascone C, Pollio A (2007) Species composition of Cyanidiales assemblages in Pisciarelli (Campi Flegrei, Italy) and description of Galdieria phlegrea sp. nov. In: Seckbach J (ed) Algae and Cyanobacteria in Extreme Environments. Springer, Dordrecht, pp 487–502

    Google Scholar 

  • Podola B, Li T, Melkonian M (2017) Porous substrate bioreactors: a paradigm shift in microalgal biotechnology? Trends Biotechnol 35:121–132

    CAS  PubMed  Google Scholar 

  • Richmond A, Qiang H (2010) Principles for efficient utilization of light for mass production of photoautotrophic microorganisms. Appl Biochem Biotechnol 65:649–658

    Google Scholar 

  • Richmond A, Lichtenberg E, Stahl B, Vonshak A (1990) Quantitative assessment of the major limitations on productivity of Spirulina platensis in open raceways. J Appl Phycol 2:195–206

    Google Scholar 

  • Rimbau V, Camins A, Romay C, Gonzalez R, Pallas M (1999) Protective effects of C-phycocyanin against kainic acid-induced neuronal damage in rat hippocampus. Neurosci Lett 276:75–78

    CAS  PubMed  Google Scholar 

  • Rizwan M, Mujtaba G, Memon SA, Lee K, Rashid N (2018) Exploring the potential of microalgae for new biotechnology applications and beyond: a review. Renew Sust Energ Rev 92:394–404

    Google Scholar 

  • 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 4:207–216

    CAS  PubMed  Google Scholar 

  • Santos R, Santos P, Santos C, Dantas F, Teixera C (2019) Evaluation of the co-production of total carotenoids, C-phycocyanin and polyhydroxyalkanoates by Arthrospira platensis. Bioresour Technol Rep 7:30–35

    Google Scholar 

  • Schmidt RA, Wiebe MG, Eriksen NT (2005) Heterotrophic high cell-density fed-batch cultures of the phycocyanin producing red alga Galdieria sulphuraria. Biotechnol Bioeng 90:77–84

    CAS  PubMed  Google Scholar 

  • Schultze LKP, Simon MV, Li T, Langenbach D, Podola B, Melkonian M (2015) High light and carbon dioxide optimize surface productivity in a twin-layer biofilm photobioreactor. Algal Res 8:37–44

    Google Scholar 

  • Seckbach J (ed) (2007) Algae and Cyanobacteria in extreme environments. Springer, Dordrecht, The Netherlands

    Google Scholar 

  • Seckbach J, Chapman DJ (eds) (2010) Red algae in the genomic age. Springer, Dordrecht, The Netherlands

    Google Scholar 

  • Shi J, Podola B, Melkonian M (2007) Removal of nitrogen and phosphorus from wastewater using microalgae immobilized on twin layers: an experimental study. J Appl Phycol 19:417–423

    CAS  Google Scholar 

  • Shi J, Podola B, Melkonian M (2014) Application of a prototype-scale twin-layer photobioreactor for effective N and P removal from different process stages of municipal wastewater by immobilized microalgae. Bioresour Technol 154:260–266

    CAS  PubMed  Google Scholar 

  • da Silva VB, Moreira JB, de Morais MG, Costa JAV (2016) Microalgae as a new source of bioactive compounds in food supplements. Curr Opin Food Sci 7:73–77

    Google Scholar 

  • Sloth JK, Wiebe MG, Eriksen NT (2006) Accumulation of phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzym Microb Technol 38:168–175

    CAS  Google Scholar 

  • Sloth JK, Jensen H, Pleissner D, Eriksen N (2017) Growth and phycocyanin synthesis in the heterotrophic microalga Galdieria sulphuraria on substrates made of food waste from restaurants and bakeries. Bioresour Technol 238:296–305

    CAS  PubMed  Google Scholar 

  • Sørensen L, Hantke A, Eriksen NT (2013) Purification of the photosynthetic pigment C-phycocyanin from heterotrophic Galdieria sulphuraria. J Sci Food Agric 93:2933–2938

    PubMed  Google Scholar 

  • Sosa-Hernández JE, Rodas Zuluaga LI, Castillo-Zacarías C, Rostro-Alanís M, de la Cruz R, Carrillo-Nieves D, Lovitt RW (2019a) A Light intensity and nitrogen concentration impact on the biomass and phycoerythrin production by Porphyridium purpureum. Mar Drugs 17:460

    PubMed Central  Google Scholar 

  • Sosa-Hernández JE, Romero-Castillo KD, Parra-Arroyo L, Aguilar-Aguila-Isaías MA, García-Reyes IE, Ahmed I, Iqbal H (2019b) Mexican microalgae biodiversity and state-of-the-art extraction strategies to meet sustainable circular economy challenges: high-value compounds and their applied perspectives. Mar Drugs 17:174–178

    PubMed Central  Google Scholar 

  • Takano H, Arai T, Hirano M, Matsunaga T (1995) Effects of intensity and quality of light on phycocyanin production by a marine cyanobacterium Synechococcus sp. NKBJ 042902. Appl Microbiol Biotechnol 43:1014–1018

    CAS  Google Scholar 

  • Toplin JA, Norris TB, Lehr CR, McDermott TR, Castenholz RW (2008) Biogeographic and phylogenetic diversity of thermoacidophilic Cyanidiales in Yellowstone National Park, Japan and New Zealand. Appl Environ Microbiol 74:2822–2833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vernes L, Granvillain P, Chemat F, Vian M (2015) Phycocyanin from Arthrospira platensis. Production, extraction and analysis. Curr Biotechnol 4:481–491

    CAS  Google Scholar 

  • Wan I, Minxi U, Zhenyang W, Zhen Z, Jun W, Shulan L, Anquan Y, Yuanguang L (2016) A novel paradigm for the high-efficient production of phycocyanin from Galdieria sulphuraria. Bioresour Technol 218:272–278

    CAS  PubMed  Google Scholar 

  • Wang J, Liu J, Liu T (2015) The difference in effective light penetration may explain the superiority in photosynthetic efficiency of attached cultivation over the conventional open pond for microalgae. Biotechnol Biofuels 26:8–49

    CAS  Google Scholar 

  • Xie Y, Jin Y, Zeng X, Chen J, Lu Y, Jing K (2015) Fed-batch strategy for enhancing cell growth and C-phycocyanin production of Arthrospira (Spirulina) platensis under phototrophic cultivation. Bioresour Technol 180:281–285

    CAS  PubMed  Google Scholar 

  • Yamanaka G, Glazer A (1980) Dynamic aspects of phycobilisome structure. Arch Microbiol 124:39–47

    CAS  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    CAS  PubMed  Google Scholar 

  • Yu J, Hancui H, Xiadoan H, Congchun W, Ting Z, Yuhan L. Roger R, Hongli Z (2019) Continuous cultivation of Arthrospira platensis for phycocyanin production in large-scale outdoor raceway ponds using microfiltered culture medium. Bioresour Technol 287:121420

    CAS  PubMed  Google Scholar 

  • Zhuang L, Dawei Y, Zhang J, Fei L, Yin W, Tian Z, Guo H, Hong Y (2018) The characteristics and influencing factors of the attached microalgae cultivation: a review. Renew Sust Energ Rev 94:1110–1119

    CAS  Google Scholar 

  • Zuccaro G, Steyer JP, Van Lis R (2019) The algal trophic mode affects the interaction and oil production of a synergistic microalga-yeast consortium. Bioresour Technol 237:608–617

    Google Scholar 

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Carbone, D.A., Olivieri, G., Pollio, A. et al. Biomass and phycobiliprotein production of Galdieria sulphuraria, immobilized on a twin-layer porous substrate photobioreactor. Appl Microbiol Biotechnol 104, 3109–3119 (2020). https://doi.org/10.1007/s00253-020-10383-8

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