Phycobiliproteins as Food Additives

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Abstract

The phycobiliproteins (FBPs) are antenna pigments composed of apoprotein covalently bound to phycobilin (tetrapyrrole chain chromophores). The main FBPs are phycoerythrin (PE), phycocyanin (PC), and allophycocyanin (APC) that absorb at 550, 620, and 650 nm, respectively, and are associated with phycobilisomes in cyanobacteria and rhodophytes. At present, it is of industrial-biotechnological interest to use natural dyes mainly blue pigments with food grade quality. The main known source is phycocyanin (PC) although unstable for use in industrial food processes because it degrades at temperatures above 45 °C and it is sensible to light and pH. Recently, it was reported that some extremophile microorganisms, such as the thermophilic red algae Cyanidioschyzon merolae, are able to produce PC which is stable to pH 5 at 83 °C, but with a half-lifetime of 40 min. Another interesting example is a halophylic cyanobacteria Euhalothece sp. that can grow at 45 °C, pH 6–9, and 12% NaCl which allows low risk of microbial contamination. The PC from this cyanobacteria was purified up to analytical grade (purity >2) and was stable at 45 °C, pH 5–8. These strains open the possibility to explore more biotechnological conditions that would allow to generate a pigment with a longer half time for industrial use. The last studies about phycobiliproteins have been focused on the way to prevent the loss of color due to PC degradation. In this regard several preservatives substances were tested such as citric acid, fructose, beet pectin, crosslinking with methylglyoxal (MGO). Formulation in anionic micelles was also investigated. The PC from Spirulina platensis improved its stability in the presence of citric acid (4 mg/mL) at 35 °C during 15 days. It has been shown a correlation between sugars (mainly fructose) and PC stability, but the use is limited for pastry and confectionery due to the high sugar content. On the other hand Sodium Dodecyl Sulfate micelles stabilize the non-protonated (blue) forms of PC and prevent the formation of protonated forms (green) at low pH. The challenge in the field of phycobiliproteins is to improve the stability at high temperatures for its use in food in order to guarantee food safety and overall quality. This can be achieved by using genetic, molecular tools and biotechnological approaches including extremophile microorganisms.

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References

  • Antelo, F. S., Costa, J. A. V., & Kalil, S. J. (2008). Thermal degradation kinetics of the phycocyanin from spirulina platensis. Biochemical Engineering Journal, 41(1), 43–47. https://doi.org/10.1016/j.bej.2008.03.012.

    Article  CAS  Google Scholar 

  • Berks, D. S., Crespi, H. L., & Katz, J. J. (1963). Isolation, amino acid composition and some physico-chemical properties of the protein deuterio-phycocyanin. Journal of the American Chemical Society, 85(1), 8–14. https://doi.org/10.1021/ja00884a002.

    Article  Google Scholar 

  • Chaiklahan, R., Chirasuwan, N., & Bunnag, B. (2012). Stability of phycocyanin extracted from spirulina sp.: Influence of temperature, pH and preservatives. Process Biochemistry, 47(4), 659–664. https://doi.org/10.1016/j.procbio.2012.01.010.

  • Chen, C.-H., Roth, L. G., MacColl, R., & Berns, D. S. (1994). Thermodynamics elucidation of the structural stability of a thermophilic protein. Biophysical Chemistry, 50(3), 313–321. https://doi.org/10.1016/0301-4622(93)E0102-B.

  • Choi, W. Y., & Lee, H. Y. (2018). Kinetic analysis of stabilizing C-phycocyanin in the spirulina platensis extracts from ultrasonic process associated with effects of light and temperature. Applied Sciences, 8(9). https://doi.org/10.3390/app8091662 (Switzerland).

  • Couteau, C., Baudry, S., Roussakis, C., & Coiffard, L. J. M. (2004). Study of thermodegradation of phycocyanin from spirulina platensis. Sciences Des Aliments, 24(5), 415–421.

    Article  CAS  Google Scholar 

  • Dewi, E. N., Kurniasih, R. A., & Purnamayati, L. (2018). The application of microencapsulated phycocyanin as a blue natural colorant to the quality of jelly candy. Paper presented at the IOP Conference Series: Earth and Environmental Science, 116(1). https://doi.org/10.1088/1755-1315/116/1/012047.

  • Dewi, E. N., Purnamayati, L., & Kurniasih, R. A. (2017). Physical characteristics of phycocyanin from spirulina microcapsules using different coating materials with freeze drying method. Paper presented at the IOP Conference Series: Earth and Environmental Science, 55(1). https://doi.org/10.1088/1755-1315/55/1/012060.

  • Edwards, M. R., Hauer, C., Stack, R. F., Eisele, L. E., & MacColl, R. (1997). Thermophilic C-phycocyanin: Effect of temperature, monomer stability, and structure. Biochimica Et Biophysica Acta—Bioenergetics, 1321(2), 157–164. https://doi.org/10.1016/S0005-2728(97)00056-X.

    Article  CAS  Google Scholar 

  • Eisele, L. E., Bakhru, S. H., Liu, X., MacColl, R., & Edwards, M. R. (2000). Studies on C-phycocyanin from cyanidium caldarium, a eukaryote at the extremes of habitat. Biochimica Et Biophysica Acta-Bioenergetics, 1456(2–3), 99–107. https://doi.org/10.1016/S0005-2728(99)00110-3.

    Article  CAS  Google Scholar 

  • Falkeborg, M. F., Roda-Serrat, M. C., Burnæs, K. L., & Nielsen, A. L. D. (2018). Stabilising phycocyanin by anionic micelles. Food Chemistry, 239, 771–780. https://doi.org/10.1016/j.foodchem.2017.07.007.

    Article  CAS  PubMed  Google Scholar 

  • Gantt, E., & Conti, S. F. (1966). Granules associated with the chloroplast lamellae of porphyridium cruentum. The Journal of Cell Biology, 29(3), 423–434. https://doi.org/10.1083/jcb.29.3.423.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadiyanto, Christwardana, M., Sutanto, H., Suzery, M., Amelia, D., & Aritonang, R. F. (2018). Kinetic study on the effects of sugar addition on the thermal degradation of phycocyanin from spirulina sp. Food Bioscience, 22, 85–90. https://doi.org/10.1016/j.fbio.2018.01.007.

  • Hayashi, N. R., Terazono, K., Hasegawa, N., Kodama, T., & Igarashi, Y. (1997). Identification and characterization of phycobiliprotein from a thermophilic cyanobacterium, chroococcidiopsis sp. strain TS-821. Journal of Fermentation and Bioengineering, 84(5), 475–477. https://doi.org/10.1016/S0922-338X(97)82011-9.

  • Kannaujiya, V. K., & Sinha, R. P. (2016). Thermokinetic stability of phycocyanin and phycoerythrin in food-grade preservatives. Journal of Applied Phycology, 28(2), 1063–1070. https://doi.org/10.1007/s10811-015-0638-x.

    Article  CAS  Google Scholar 

  • Kaur, S., Khattar, J. I. S., Singh, Y., Singh, D. P., & Ahluwalia, A. S. (2019). Extraction, purification and characterisation of phycocyanin from anabaena fertilissima PUPCCC 410.5: As a natural and food grade stable pigment. Journal of Applied Phycology. https://doi.org/10.1007/s10811-018-1722-9.

  • Khazi, M. I., Demirel, Z., & Dalay, M. C. (2018). Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. Journal of Applied Phycology, 30(3), 1513–1523. https://doi.org/10.1007/s10811-018-1398-1.

    Article  CAS  Google Scholar 

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

  • Larrosa, A. P. Q., Camara, Á. S., Pohndorf, R. S., da Rocha, S. F., & Pinto, L. A. A. (2018). Physicochemical, biochemical, and thermal properties of arthrospira (spirulina) biomass dried in spouted bed at different conditions. Journal of Applied Phycology, 30(2), 1019–1029. https://doi.org/10.1007/s10811-017-1265-5.

    Article  CAS  Google Scholar 

  • Leu, J.-Y., Lin, T.-H., Selvamani, M. J. P., Chen, H.-C., Liang, J.-Z., & Pan, K.-M. (2013). Characterization of a novel thermophilic cyanobacterial strain from Taian hot springs in Taiwan for high CO2 mitigation and C-phycocyanin extraction. Process Biochemistry, 48(1), 41–48. https://doi.org/10.1016/j.procbio.2012.09.019.

  • Liang, Y., Kaczmarek, M. B., Kasprzak, A. K., Tang, J., Shah, M. M. R., **, P., et al. (2018). Thermosynechococcaceae as a source of thermostable C-phycocyanins: Properties and molecular insights. Algal Research, 35, 223–235. https://doi.org/10.1016/j.algal.2018.08.037.

  • Martelli, G., Folli, C., Visai, L., Daglia, M., & Ferrari, D. (2014). Thermal stability improvement of blue colorant C-phycocyanin from spirulina platensis for food industry applications. Process Biochemistry, 49(1), 154–159. https://doi.org/10.1016/j.procbio.2013.10.008.

    Article  CAS  Google Scholar 

  • Mishra, S. K., Shrivastav, A., & Mishra, S. (2008). Effect of preservatives for food grade C-PC from spirulina platensis. Process Biochemistry, 43(4), 339–345. https://doi.org/10.1016/j.procbio.2007.12.012.

    Article  CAS  Google Scholar 

  • Mishra, S. K., Shrivastav, A., Pancha, I., Jain, D., & Mishra, S. (2010). Effect of preservatives for food grade C-phycoerythrin, isolated from marine cyanobacteria pseudanabaena sp. International Journal of Biological Macromolecules, 47(5), 597–602. https://doi.org/10.1016/j.ijbiomac.2010.08.005.

    Article  CAS  PubMed  Google Scholar 

  • Mogany, T., Kumari, S., Swalaha, F. M., & Bux, F. (2018). Extraction and characterisation of analytical grade C-phycocyanin from euhalothece sp. Journal of Applied Phycology. https://doi.org/10.1007/s10811-018-1661-5.

    Article  Google Scholar 

  • Munawaroh, H. S. H., Darojatun, K., Gumilar, G. G., Aisyah, S., & Wulandari, A. P. (2018). Characterization of phycocyanin from spirulina fusiformis and its thermal stability. Paper presented at the Journal of Physics: Conference Series, 1013(1). https://doi.org/10.1088/1742-6596/1013/1/012205.

  • Murthy, S. D. S., Ramanaiah, V. V., & Sudhir, P. (2004). High temperature induced alterations in energy transfer in phycobilisomes of the cyanobacterium spirulina platensis. Photosynthetica, 42(4), 615–617. https://doi.org/10.1007/S11099-005-0021-2.

    Article  CAS  Google Scholar 

  • Pan-utai, W., Kahapana, W., & Iamtham, S. (2018). Extraction of C-phycocyanin from arthrospira (spirulina) and its thermal stability with citric acid. Journal of Applied Phycology, 30(1), 231–242. https://doi.org/10.1007/s10811-017-1155-x.

    Article  CAS  Google Scholar 

  • Patel, A., Pawar, R., Mishra, S., Sonawane, S., & Ghosh, P. K. (2004). Kinetic studies on thermal denaturation of C-phycocyanin. Indian Journal of Biochemistry and Biophysics, 41(5), 254–257.

    CAS  PubMed  Google Scholar 

  • Pumas, C., Peerapornpisal, Y., Vacharapiyasophon, P., Leelapornpisid, P., Boonchum, W., Ishii, M., et al. (2012). Purification and characterization of a thermostable phycoerythrin from hot spring cyanobacterium leptolyngbya sp. KC45. International Journal of Agriculture and Biology, 14(1), 121–125.

    Google Scholar 

  • Pumas, C., Vacharapiyasophon, P., Peerapornpisal, Y., Leelapornpisid, P., Boonchum, W., Ishii, M., & Khanongnuch, C. (2011). Thermostablility of phycobiliproteins and antioxidant activity from four thermotolerant cyanobacteria. Phycological Research, 59(3), 166–174. https://doi.org/10.1111/j.1440-1835.2011.00615.x.

    Article  CAS  Google Scholar 

  • Purnamayati, L., Dewi, E. N., & Kurniasih, R. A. (2018). Phycocyanin stability in microcapsules processed by spray drying method using different inlet temperature. Paper presented at the IOP Conference Series: Earth and Environmental Science, 116(1). https://doi.org/10.1088/1755-1315/116/1/012076.

  • Rahman, D. Y., Sarian, F. D., van Wijk, A., Martinez-Garcia, M., & van der Maarel, M. J. E. C. (2017). Thermostable phycocyanin from the red microalga cyanidioschyzon merolae, a new natural blue food colorant. Journal of Applied Phycology, 29(3), 1233–1239. https://doi.org/10.1007/s10811-016-1007-0.

    Article  CAS  PubMed  Google Scholar 

  • Rastogi, R. P., Sonani, R. R., & Madamwar, D. (2015). Physico-chemical factors affecting the in vitro stability of phycobiliproteins from phormidium rubidum A09DM. Bioresource Technology, 190, 219–226. https://doi.org/10.1016/j.biortech.2015.04.090.

    Article  CAS  PubMed  Google Scholar 

  • Rippka, R., Deruelles, J., & Waterbury, J. B. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology, 111(1), 1–61.

    Google Scholar 

  • Sala, L., Moraes, C. C., & Kalil, S. J. (2018). Cell pretreatment with ethylenediaminetetraacetic acid for selective extraction of C-phycocyanin with food grade purity. Biotechnology Progress, 34(5), 1261–1268. https://doi.org/10.1002/btpr.2713.

    Article  CAS  PubMed  Google Scholar 

  • Samsonoff, W. A., & MacColl, R. (2001). Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Archives of Microbiology, 176(6), 400–405. https://doi.org/10.1007/s002030100346.

    Article  CAS  PubMed  Google Scholar 

  • Seibert, M., & Connolly, J. S. (1984). Fluorescence properties of C-phycocyanin isolated from a thermophilic cyanobacterium. Photochemistry and Photobiology, 40(2), 267–271. https://doi.org/10.1111/j.1751-1097.1984.tb04585.x.

    Article  CAS  Google Scholar 

  • Selig, M. J., Malchione, N. M., Gamaleldin, S., Padilla-Zakour, O. I., & Abbaspourrad, A. (2018). Protection of blue color in a spirulina derived phycocyanin extract from proteolytic and thermal degradation via complexation with beet-pectin. Food Hydrocolloids, 74, 46–52. https://doi.org/10.1016/j.foodhyd.2017.07.027.

    Article  CAS  Google Scholar 

  • Singh, N. K., Parmar, A., Sonani, R. R., & Madamwar, D. (2012). Isolation, identification and characterization of novel thermotolerant oscillatoria sp. N9DM: Change in pigmentation profile in response to temperature. Process Biochemistry, 47(12), 2472–2479. https://doi.org/10.1016/j.procbio.2012.10.009.

  • Tandeau de Marsac, N., & Houmard, J. (1993). Adaptation of cyanobacteria to environmental stimuli: New steps towards molecular mechanisms. FEMS Microbiology Letters, 104(1–2), 119–189. https://doi.org/10.1016/0378-1097(93)90506-W.

    Article  CAS  Google Scholar 

  • Topchishvili, L. S., Barbakadze, S. I., Khizanishvili, A. I., Majagaladze, G. V., & Monaselidze, J. R. (2002). Microcalorimetric study iodized and noniodized cells and C-phycocyanin of spirulina platensis. Biomacromolecules, 3(3), 415–420. https://doi.org/10.1021/bm0155928.

    Article  CAS  PubMed  Google Scholar 

  • Tripathi, S. N., Kapoor, S., & Shrivastava, A. (2007). Extraction and purification of an unusual phycoerythrin in a terrestrial desiccation tolerant cyanobacterium lyngbya arboricola. Journal of Applied Phycology, 19(5), 441–447. https://doi.org/10.1007/s10811-006-9151-6.

    Article  CAS  Google Scholar 

  • Wu, H.-L., Wang, G.-H., **ang, W.-Z., Li, T., & He, H. (2016). Stability and antioxidant activity of food-grade phycocyanin isolated from spirulina platensis. International Journal of Food Properties, 19(10), 2349–2362. https://doi.org/10.1080/10942912.2015.1038564.

    Article  CAS  Google Scholar 

  • Zhao, J., & Brand, J. J. (1989). Specific bleaching of phycobiliproteins from cyanobacteria and red algae at high temperature in vivo. Archives of Microbiology, 152(5), 447–452. https://doi.org/10.1007/BF00446927.

    Article  CAS  Google Scholar 

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Acknowledgements

Universidad de Antofagasta, Chile Grant number Semillero de Investigación, SI-5305 and CeBiB Grant number FB0001 (CONICYT, Chile).

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Correspondence to Laurent Dufossé .

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Alexandra Galetović C., Dufossé, L. (2020). Phycobiliproteins as Food Additives. In: Jacob-Lopes, E., Queiroz, M., Zepka, L. (eds) Pigments from Microalgae Handbook. Springer, Cham. https://doi.org/10.1007/978-3-030-50971-2_22

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