Abstract
Pigments are present in a broad variety of terrestrial and aquatic organisms. The cannonball jellyfish (Stomolophus sp. 2) is an important fishery resource in the northwest of Mexico and is processed to be traded and consumed as seafood. During the process, water with a soluble blue pigment and other compounds are discarded to the environment. In this work, we present some properties of the blue pigment from Stomolophus sp.2 (S2bp), to decide if it could be considered as a potential value-added waste and avoid the blue proteinaceous pigment wastewater. S2bp was purified to homogeneity and had a molecular mass of 28.0 kDa; this protein exhibited a ʎmax at 650 nm, contained Zn2+ and Cu2+ metal ions, and was stable from 10 to 50 °C and in a pH range of 3.0 to 13.0 for 1 h. It had halotolerant characteristics maintaining the blue coloration in a broad range of ionic strength (0–4 M NaCl) and showed changes in ʎmax with chaotropic salts. In addition, S2bp was stable in the presence of organic acids and EDTA and in zwitterionic, anionic, and nonionic detergents at critical micellar concentration. However, oxidant reagents like NaClO and H2O2 decrease the coloration. These results show that the jellyfish pigment is a stable protein which makes it an alternative pigment for the food industry.
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References
Alvaréz-Gutierrez JM (2013) Establecimiento de indicadores de calidad y deterioro en el músculo de lisa rayada (Mugil cephalus) y campana de medusa bala de cañón (Stomolophus meleagris). Master in Science in Natural Resourses´ thesis. Instituto Tecnológico de Sonora
Amado IR, Vázquez JA, Murado MA, González MP (2015) Recovery of astaxanthin from shrimp cooking wastewater: optimization of astaxanthin extraction by response surface methodology and kinetic studies. Food Bioprocess Technol 8:371–381. https://doi.org/10.1007/s11947-014-1403-x
Barbier M (1982) Calliactine, a paramagnetic violet pigment from the sea anemone Calliactis parasitica. Naturwissenschaften 69:341–342. https://doi.org/10.1007/bf00480459
Blanquet RS, Phelan MA (1987) An unusual blue mesogleal protein from the mangrove jellyfish Cassiopea xamachana. Mar Biol 94:423–430. https://doi.org/10.1007/BF00428249
Bogár F, Bartha F, Násztor Z, Fábián L, Leitgeb B, Dér A (2014) On the Hofmeister effect: fluctuations at the protein–water Interface and the surface tension. J Phys Chem B 118:8496–8504. https://doi.org/10.1021/jp502505c
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Britton G (1983) The biochemistry if natural pigments. Cambridge University Press, Cambridge
Bulina ME, Lukyanov KA, Yampolsky IV, Chudakov DM, Staroverov DB, Shcheglov AS, Gurskaya NG, Lukyanov S (2004) New class of blue animal pigments based on Frizzled and Kringle protein domains. J Biol Chem 279:43367–43370. https://doi.org/10.1074/jbc.C400337200
Cariello L, Zanetti L (1981) A blue carotenoprotein from the marine sponge Suberites domuncula: purification and properties. Mar Biol 62:151–155. https://doi.org/10.1007/bf00388177
Chaiklahan R, Chirasuwan N, Bunnag B (2012) Stability of phycocyanin extracted from Spirulina sp.: influence of temperature, pH and preservatives. Process Biochem 47:659–664. https://doi.org/10.1016/j.procbio.2012.01.010
Christomanos A (1953) Purple pigment and protein in the threads of the sea anemone, Adamsia rondeleti. Nature 171:886–887. https://doi.org/10.1038/171886b0
Cristea D, Vilarem G (2006) Improving light fastness of natural dyes on cotton yarn. Dyes Pigments 70:238–245. https://doi.org/10.1016/j.dyepig.2005.03.006
Cruz-Colín ME, Cisneros-Mata MÁ, Montaño-Moctezuma G (2019) Análisis de actores de la pesquería de medusa en Guaymas. Sonora Reg Soc 31
Dove SG, Takabayashi M, Hoegh-Guldberg O (1995) Isolation and partial characterization of the pink and blue pigments of Pocilloporid and Acroporid corals. Biol Bull 189:288–297. https://doi.org/10.2307/1542146
Ferrari M, Folli C, Pincolini E, McClintock TS, Rössle M, Berni R, Cianci M (2012) Structural characterization of recombinant crustacyanin subunits from the lobster Homarus americanus. Acta Crystallogr Sect F 68:846–853. https://doi.org/10.1107/s1744309112026103
Galanakis CM, Tsatalas P, Galanakis IM (2018) Implementation of phenols recovered from olive mill wastewater as UV booster in cosmetics. Ind Crop Prod 111:30–37. https://doi.org/10.1016/j.indcrop.2017.09.058
Gastineau R et al (2012) Biological activities of purified marennine, the blue pigment responsible for the greening of oysters. J Agric Food Chem 60:3599–3605. https://doi.org/10.1021/jf205004x
Gómez Daglio L, Dawson MN (2017) Species richness of jellyfishes (Scyphozoa: Discomedusae) in the Tropical Eastern Pacific: missed taxa, molecules, and morphology match in a biodiversity hotspot. Invertebr Syst 31:635–663. https://doi.org/10.1071/IS16055
Graziano G, Merlino A (2014) Molecular bases of protein halotolerance. Biochim Biophys Acta, Proteins Proteomics 1844:850–858. https://doi.org/10.1016/j.bbapap.2014.02.018
Helgason T, Bohn B, Weiland A, Sowa C, Gottschalk T (2015) Stabilized phycocyanin for blue color. Germany (DE) Patent
Jespersen L, Strømdahl LD, Olsen K, Skibsted LH (2005) Heat and light stability of three natural blue colorants for use in confectionery and beverages. Eur Food Res Technol 220:261–266. https://doi.org/10.1007/s00217-004-1062-7
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Li J, Liang L, Cheng J, Huang Y, Zhu M, Liang S (2012) Extraction of pigment from sugarcane juice alcohol wastewater and evaluation of its antioxidant and free radical scavenging activities. Food Sci Biotechnol 21:1489–1496. https://doi.org/10.1007/s10068-012-0197-8
López-Martínez J, Álvarez-Tello J (2013) The jellyfish fishery in Mexico. Agric Sci 4:57–61
Lugo-Magaña O, García XG, Barrientos RG, Legarreta IG (2018) Preliminary characterization of a blue pigment extracted from “cannon ball” jellyfish Stomolophus meleagris. Russ J Mar Biol 44:477–483. https://doi.org/10.1134/S1063074018060081
Merril CR, Washart KM (1998) Gel electrophoresis of proteins: a practical approach. Oxford University Press, New York
Moradi N, Salem S, Salem A (2018) Optimizing adsorption of blue pigment from wastewater by nano-porous modified Na-bentonite using spectrophotometry based on response surface method. Spectrochim Acta A Mol Biomol Spectrosc 193:54–62. https://doi.org/10.1016/j.saa.2017.12.010
Nazneen S, Polugari R, Raj S, Singh P (2015) Comparative study on effect of different capping agents on the antimicrobial activity of ZnoO nanoparticles. Int J Pharm Sci Res 6:4022–4025
Peng W, Fan X, Wang S, Zhang G, Zhang F (2010) A novel method for the recovery of 4,4′-dinitrostilbene-2,2′disulfonic acid from the wastewater obtained from 4,4′-diaminostilbene-2,2′-disulfonic acid production. Dyes Pigments 84:218–222. https://doi.org/10.1016/j.dyepig.2009.09.005
Reddy A, Norris DF, Momeni SS, Waldo B, Ruby JD (2016) The pH of beverages in the United States. J Am Dent Assoc 147:255–263. https://doi.org/10.1016/j.adaj.2015.10.019
Rhee SG, Bae YS, Lee S-R, Kwon J (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000:pe1. https://doi.org/10.1126/stke.2000.53.pe1
Russell NJ, Gould GW (2003) Food preservatives. Springer US, New York
Stauffer C (1989) Enzyme assays for food scientist. New York
Venil CK, Zakaria ZA, Ahmad WA (2013) Bacterial pigments and their applications. Process Biochem 48:1065–1079. https://doi.org/10.1016/j.procbio.2013.06.006
Walker JM (1996) The bicinchoninic acid (BCA) assay for protein quantitation. In: Walker JM (ed) The protein protocols handbook. Humana Press, Totowa, pp 11–14. https://doi.org/10.1007/978-1-60327-259-9_3
Wu Z, Zhong H, Yuan X, Wang H, Wang L, Chen X, Zeng G, Wu Y (2014) Adsorptive removal of methylene blue by rhamnolipid-functionalized graphene oxide from wastewater. Water Res 67:330–344. https://doi.org/10.1016/j.watres.2014.09.026
Wu H-L, Wang G-H, Xiang W-Z, Li T, He H (2016) Stability and antioxidant activity of food-grade Phycocyanin isolated from Spirulina platensis. Int J Food Prop 19:2349–2362. https://doi.org/10.1080/10942912.2015.1038564
Zhang H, Zhan J, Su K, Zhang Y (2006) A kind of potential food additive produced by Streptomyces coelicolor: characteristics of blue pigment and identification of a novel compound, k-actinorhodin. Food Chem 95:186–192
Zhao Y et al (2011) Astaxanthin preparation by lipase-catalyzed hydrolysis of its esters from Haematococcus pluvialis. Algal Extracts. J Food Sci 76:C643–C650. https://doi.org/10.1111/j.1750-3841.2011.02119.x
Acknowledgments
We thank Luis Enrique Ordaz Cruz and Manuel Kirchmayr from CIATEJ for the support with MALDI-TOF analysis, Abigail Hernández for the jellyfish samples, Alicia Verónica Camacho Pacheco for the Stomolophus sp. 2 photographs, and Claudia Maytorena for her comments to improve the manuscript.
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Martínez-Pérez, R.B., Díaz-Tenorio, L.M., Leyva Soto, L.A. et al. Characterization of cannonball jellyfish (Stomolophus sp. 2) blue protein: a pH-stable pigment. Environ Sci Pollut Res 27, 28597–28606 (2020). https://doi.org/10.1007/s11356-020-08689-1
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DOI: https://doi.org/10.1007/s11356-020-08689-1