A review of the nutritional and medicinal potential of Phycobiliproteins extracted from cyanobacteria
Subject Areas : Food HygieneBahareh Nowruzi 1 , yasaman Gorani 2
1 - Department of Biotechnology, Faculty of Converging Sciences and Technologies, Islamic Azad University, Science and Research Branch, Tehran, Iran
2 - M.Sc. Student of Industrial Microbiology, Faculty of Converging Sciences and Technologies, Islamic Azad University, Science and Research Branch, Tehran, Iran
Keywords: Phycocyanin, Phycobiliproteins, medicinal potential, food pigments,
Abstract :
Phycobiliproteins (PBPs) are colored and water-soluble biliproteins that are found in cyanobacteria and rhodophytes. Based on their spectral characteristics, PBPs are divided into three types: Allophycocyanin, phycocyanin and phycoerythrin. PBPs, apart from their special function as sunlight-receiving antennas in the photosynthesis process, can be used as food dyes, nutrients, cosmetics, pharmaceutical industries and fluorescent probes in immunofluorescence analysis. Since PBPs have antioxidant, anti-tumor effects, as well as potential anti-inflammatory and anti-diabetic properties, in this review article, an attempt was made to investigate the properties and medicinal potential of PBPs along with their structural features. The results of the review of recent articles showed that the PBP part of proteins is very sensitive to environmental stress and this issue limits their use in the food industry. Therefore, it is necessary to use protective and coating materials to preserve the color. Consequently, they can prevent the denaturation of the protein structure, which not only increases the antioxidant properties but also increases the half-life of the food.
References:
Adir, N., Bar-Zvi, S. and Harris, D. )2020(. The amazing phycobilisome. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1861(4):
Anvar, S.A.A. and Nowruzi, B. (2021). A review of phycobiliproteins of cyanobacteria: structure, function and industrial applications in food and pharmaceutical industries. Research and Innovation in Food Science and Technology, 10(2): 181-198.
Anvar, S.A.A., Nowruzi, B. and Afshari, G. (2022). A Review of the Application of Nanoparticles Biosynthesized by Microalgae and Cyanobacteria in Medical and Veterinary Sciences. Iranian Journal of Veterinary Medicine, 17(1): 1-18.
Asadollahi, A. and Nowruzi, B. (2023). A review of different methods of skin care using cyanobacteria. Journal of Dermatology and Cosmetic, 13(4): 285-299.
Ashaolu, T.J., Samborska, K., Lee, C.C., Tomas, M., Capanoglu, E., Tarhan, Ö. et al., (2021). Phycocyanin, a super functional ingredient from algae; properties, purification characterization, and applications. International Journal of Biological Macromolecules, 193: 2320-2331.
Basheva, D., Moten, D., Stoyanov, P., Belkinova, D., Mladenov, R. and Teneva, I. (2018). Content of phycoerythrin, phycocyanin, alophycocyanin and phycoerythrocyanin in some cyanobacterial strains: Applications. Engineering in Life Sciences, 18(11): 861-866.
Chen, H., Qi, H. and Xiong, P. (2022). Phycobiliproteins—a Family of Algae-Derived Biliproteins: Productions, Characterization and Pharmaceutical Potentials. Marine Drugs, 20(7): 450.
Dagnino-Leone, J., Figueroa, C.P., Castañeda, M.L., Youlton, A.D., Vallejos-Almirall, A., Agurto-Muñoz, A. et al., (2022). Phycobiliproteins: Structural aspects, functional characteristics, and biotechnological perspectives. Computational and Structural Biotechnology Journal, 20: 1506-1527
De Morais, M.G., da Fontoura Prates, D., Moreira, J.B., Duarte, J.H. and Costa, J.A.V. (2018). Phycocyanin from microalgae: properties, extraction and purification, with some recent applications. Industrial Biotechnology, 14(1): 30-37.
Eriksen, N.T. (2008). Production of phycocyanin—a pigment with applications in biology, biotechnology, foods and medicine. Applied microbiology and biotechnology, 80: 1-14.
Ferraro, G., Imbimbo, P., Marseglia, A., Illiano, A., Fontanarosa, C., Amoresano, A. et al., (2020). A thermophilic C-phycocyanin with unprecedented biophysical and biochemical properties. International journal of biological macromolecules, 150: 38-51.
Fratelli, C., Burck, M., Amarante, M.C.A. and Braga, A.R.C. (2021). Antioxidant potential of natures “something blue”: something new in the marriage of biological activity and extraction methods applied to C-phycocyanin. Trends in Food Science & Technology, 107: 309-323.
Freitas, M.V., Pacheco, D., Cotas, J., Mouga, T., Afonso, C. and Pereira, L. (2022). Red seaweed pigments from a biotechnological perspective. Phycology, 2(1): 1-29.
Galetović, A., Seura, F., Gallardo, V., Graves, R., Cortés, J., Valdivia, C. et al., (2020). Use of phycobiliproteins from atacama cyanobacteria as food colorants in a dairy beverage prototype. Foods, 9(2): 244.
García, A.B., Longo, E. and Bermejo, R. (2021). The application of a phycocyanin extract obtained from Arthrospira platensis as a blue natural colorant in beverages. Journal of Applied Phycology, 33(5): 3059-3070.
Grover, P., Bhatnagar, A., Kumari, N., Bhatt, A.N., Nishad, D.K. and Purkayastha, J. (2021). C-Phycocyanin-a novel protein from Spirulina platensis-In vivo toxicity, antioxidant and immunomodulatory studies. Saudi journal of biological sciences, 28(3): 1853-1859.
Hsieh-Lo, M., Castillo, G., Ochoa-Becerra, M.A. and Mojica, L. (2019). Phycocyanin and phycoerythrin: Strategies to improve production yield and chemical stability. Algal Research, 42: 101600.
Imchen, T. and Singh, K.S. (2022). Marine algae colorants: Antioxidant, anti-diabetic properties and applications in food industry. Algal Research, 69: 102898.
Jafari Porzani, S., Konur, O. and Nowruzi, B. (2022). Cyanobacterial natural products as sources for antiviral drug discovery against COVID-19. Journal of Biomolecular Structure and Dynamics, 40(16): 7629-7644.
Kannaujiya, V.K., Kumar, D., Pathak, J. and Sinha, R.P. (2019). Phycobiliproteins and their commercial significance, In: Mishra, A.K., Tiwari, D.N. and Rai, A.N. (Editors), Cyanobacteria, Academic Press, pp. 207-216.
Khandual, S., Sanchez, E.O.L., Andrews, H.E. and de la Rosa, J.D.P. (2021). Phycocyanin content and nutritional profile of Arthrospira platensis from Mexico: efficient extraction process and stability evaluation of phycocyanin. BMC chemistry, 15(1): 1-13.
Khazi, M.I., Demirel, Z. and Dalay, M.C. (2018). Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. Journal of applied phycology, 30: 1513-1523.
Kissoudi, M., Sarakatsianos, I. and Samanidou, V. (2018). Isolation and purification of food‐grade C‐phycocyanin from Arthrospira platensis and its determination in confectionery by HPLC with diode array detection. Journal of separation science, 41(4): 975-981.
Kuddus, M., Singh, P., Thomas, G. and Al-Hazimi, A. (2013). Recent developments in production and biotechnological applications of C-phycocyanin. BioMed research international, 2013.
Li, W., Su, H.N., Pu, Y., Chen, J., Liu, L.N., Liu, Q. et al., (2019). Phycobiliproteins: Molecular structure, production, applications, and prospects. Biotechnology Advances, 37(2): 340-353.
Liang, Y., Kaczmarek, M.B., Kasprzak, A.K., Tang, J., Shah, M.M.R., Jin, P. et al., (2018). Thermosynechococcaceae as a source of thermostable C-phycocyanins: Properties and molecular insights. Algal research, 35: 223-235.
Ma, J., Hu, J., Sha, X., Meng, D. and Yang, R. (2022). Phycobiliproteins, the pigment-protein complex form of natural food colorants and bioactive ingredients. Critical Reviews in Food Science and Nutrition, 1-19.
Mandal, M.K., Chanu, N.K. and Chaurasia, N. (2020). Cyanobacterial pigments and their fluorescence characteristics: Applications in research and industry, In: Singh, P.K., Kumar, A., Singh, V.K and Shrivistava, A. (Editors), Advances in Cyanobacterial Biology, 1st Edition, Academic Press, pp. 55-72.
Mysliwa-Kurdziel, B. and Solymosi, K. (2017). Phycobilins and phycobiliproteins used in food industry and medicine. Mini reviews in medicinal chemistry, 17(13): 1173-1193.
Nowruzi, B. (2022). Cyanobacteria Natural Products as Sources for Future Directions in Antibiotic Drug Discovery.
Nowruzi, B., Konur, O. and Anvar, S.A.A. (2022). The stability of the phycobiliproteins in the adverse environmental conditions relevant to the food storage. Food and Bioprocess Technology, 15(12): 2646-2663.
Pagels, F., Guedes, A.C., Amaro, H.M., Kijjoa, A. and Vasconcelos, V. (2019). Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications. Biotechnology Advances, 37(3): 422-443.
Patel, S.N., Sonani, R.R., Roy, D., Singh, N.K., Subudhi, S., Pabbi, S. et al., (2022). Exploring the structural aspects and therapeutic perspectives of cyanobacterial phycobiliproteins. 3 Biotech, 12(9): 224.
Prabakaran, G., Sampathkumar, P., Kavisri, M. and Moovendhan, M. (2020). Extraction and characterization of phycocyanin from Spirulina platensis and evaluation of its anticancer, antidiabetic and antiinflammatory effect. International Journal of Biological Macromolecules, 153: 256-263.
Puzorjov, A., Dunn, K.E. and McCormick, A.J. (2021). Production of thermostable phycocyanin in a mesophilic cyanobacterium. Metabolic engineering communications, 13: e00175.
Puzorjov, A. and McCormick, A.J. (2020). Phycobiliproteins from extreme environments and their potential applications. Journal of Experimental Botany, 71(13): 3827-3842.
Qiang, X., Wang, L., Niu, J., Gong, X. and Wang, G. (2021). Phycobiliprotein as fluorescent probe and photosensitizer: A systematic review. International Journal of Biological Macromolecules, 193: 1910-1917.
Renugadevi, K., Nachiyar, C.V., Sowmiya, P. and Sunkar, S. (2018). Antioxidant activity of phycocyanin pigment extracted from marine filamentous cyanobacteria Geitlerinema sp TRV57. Biocatalysis and agricultural biotechnology, 16: 237-242.
Romay, C.H., Gonzalez, R., Ledon, N., Remirez, D. and Rimbau, V. (2003). C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Current protein and peptide science, 4(3): 207-216.
Safaei, M., Maleki, H., Soleimanpour, H., Norouzy, A., Zahiri, H.S., Vali, H. et al., (2019). Development of a novel method for the purification of C-phycocyanin pigment from a local cyanobacterial strain Limnothrix sp. NS01 and evaluation of its anticancer properties. Scientific reports, 9(1): 9474.
Saini, D.K., Pabbi, S. and Shukla, P. (2018). Cyanobacterial pigments: Perspectives and biotechnological approaches. Food and chemical toxicology, 120: 616-624.
Sauer, P.V., Dominguez-Martin, M.A., Kirst, H., Sutter, M., Bina, D., Greber, B.J. et al., (2021). Structures of the cyanobacterial phycobilisome. BioRxiv, 2021-11.
Sekar, S. and Chandramohan, M. (2008). Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. Journal of Applied Phycology, 20: 113-136.
Shafaei Bejestani, M., Anvar, A.A., Nowruzi, B. and Golestan, L. (2023). Production of cheese and ice cream enriched with biomass and supernatant of Spirulina platensis with emphasis on organoleptic and nutritional properties. Iranian Journal of Veterinary Medicine, DOI: 10.22059/IJVM.2023.355737.1005364
Sharma, R., Nath, P.C., Vanitha, K., Tiwari, O.N., Bandyopadhyay, T.K. and Bhunia, B. (2021). Effects of different monosaccharides on thermal stability of phycobiliproteins from Oscillatoria sp. (BTA-170): Analysis of kinetics, thermodynamics, colour and antioxidant properties. Food Bioscience, 44: 101354.
Vinothkanna, A. and Sekar, S. (2020). Diagnostic Applications of Phycobiliproteins. Pigments from Microalgae Handbook, 585-610.
Yuan, B., Zhuxin, L., Honghong, S., Dashnyam, B., Xiao, X., McClements, D.J., et al., (2022). A review of recent strategies to improve the physical stability of phycocyanin. Current Research in Food Science, 5: 2329-2337.
Zuorro, A., Leal-Jerez, A.G., Morales-Rivas, L.K., Mogollón-Londoño, S.O., Sanchez-Galvis, E.M., García-Martínez, J.B. et al., (2021). Enhancement of Phycobiliprotein Accumulation in Thermotolerant Oscillatoria sp. through Media Optimization. ACS omega, 6(16): 10527-10536.
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Adir, N., Bar-Zvi, S. and Harris, D. )2020(. The amazing phycobilisome. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1861(4):
Anvar, S.A.A. and Nowruzi, B. (2021). A review of phycobiliproteins of cyanobacteria: structure, function and industrial applications in food and pharmaceutical industries. Research and Innovation in Food Science and Technology, 10(2): 181-198.
Anvar, S.A.A., Nowruzi, B. and Afshari, G. (2022). A Review of the Application of Nanoparticles Biosynthesized by Microalgae and Cyanobacteria in Medical and Veterinary Sciences. Iranian Journal of Veterinary Medicine, 17(1): 1-18.
Asadollahi, A. and Nowruzi, B. (2023). A review of different methods of skin care using cyanobacteria. Journal of Dermatology and Cosmetic, 13(4): 285-299.
Ashaolu, T.J., Samborska, K., Lee, C.C., Tomas, M., Capanoglu, E., Tarhan, Ö. et al., (2021). Phycocyanin, a super functional ingredient from algae; properties, purification characterization, and applications. International Journal of Biological Macromolecules, 193: 2320-2331.
Basheva, D., Moten, D., Stoyanov, P., Belkinova, D., Mladenov, R. and Teneva, I. (2018). Content of phycoerythrin, phycocyanin, alophycocyanin and phycoerythrocyanin in some cyanobacterial strains: Applications. Engineering in Life Sciences, 18(11): 861-866.
Chen, H., Qi, H. and Xiong, P. (2022). Phycobiliproteins—a Family of Algae-Derived Biliproteins: Productions, Characterization and Pharmaceutical Potentials. Marine Drugs, 20(7): 450.
Dagnino-Leone, J., Figueroa, C.P., Castañeda, M.L., Youlton, A.D., Vallejos-Almirall, A., Agurto-Muñoz, A. et al., (2022). Phycobiliproteins: Structural aspects, functional characteristics, and biotechnological perspectives. Computational and Structural Biotechnology Journal, 20: 1506-1527
De Morais, M.G., da Fontoura Prates, D., Moreira, J.B., Duarte, J.H. and Costa, J.A.V. (2018). Phycocyanin from microalgae: properties, extraction and purification, with some recent applications. Industrial Biotechnology, 14(1): 30-37.
Eriksen, N.T. (2008). Production of phycocyanin—a pigment with applications in biology, biotechnology, foods and medicine. Applied microbiology and biotechnology, 80: 1-14.
Ferraro, G., Imbimbo, P., Marseglia, A., Illiano, A., Fontanarosa, C., Amoresano, A. et al., (2020). A thermophilic C-phycocyanin with unprecedented biophysical and biochemical properties. International journal of biological macromolecules, 150: 38-51.
Fratelli, C., Burck, M., Amarante, M.C.A. and Braga, A.R.C. (2021). Antioxidant potential of natures “something blue”: something new in the marriage of biological activity and extraction methods applied to C-phycocyanin. Trends in Food Science & Technology, 107: 309-323.
Freitas, M.V., Pacheco, D., Cotas, J., Mouga, T., Afonso, C. and Pereira, L. (2022). Red seaweed pigments from a biotechnological perspective. Phycology, 2(1): 1-29.
Galetović, A., Seura, F., Gallardo, V., Graves, R., Cortés, J., Valdivia, C. et al., (2020). Use of phycobiliproteins from atacama cyanobacteria as food colorants in a dairy beverage prototype. Foods, 9(2): 244.
García, A.B., Longo, E. and Bermejo, R. (2021). The application of a phycocyanin extract obtained from Arthrospira platensis as a blue natural colorant in beverages. Journal of Applied Phycology, 33(5): 3059-3070.
Grover, P., Bhatnagar, A., Kumari, N., Bhatt, A.N., Nishad, D.K. and Purkayastha, J. (2021). C-Phycocyanin-a novel protein from Spirulina platensis-In vivo toxicity, antioxidant and immunomodulatory studies. Saudi journal of biological sciences, 28(3): 1853-1859.
Hsieh-Lo, M., Castillo, G., Ochoa-Becerra, M.A. and Mojica, L. (2019). Phycocyanin and phycoerythrin: Strategies to improve production yield and chemical stability. Algal Research, 42: 101600.
Imchen, T. and Singh, K.S. (2022). Marine algae colorants: Antioxidant, anti-diabetic properties and applications in food industry. Algal Research, 69: 102898.
Jafari Porzani, S., Konur, O. and Nowruzi, B. (2022). Cyanobacterial natural products as sources for antiviral drug discovery against COVID-19. Journal of Biomolecular Structure and Dynamics, 40(16): 7629-7644.
Kannaujiya, V.K., Kumar, D., Pathak, J. and Sinha, R.P. (2019). Phycobiliproteins and their commercial significance, In: Mishra, A.K., Tiwari, D.N. and Rai, A.N. (Editors), Cyanobacteria, Academic Press, pp. 207-216.
Khandual, S., Sanchez, E.O.L., Andrews, H.E. and de la Rosa, J.D.P. (2021). Phycocyanin content and nutritional profile of Arthrospira platensis from Mexico: efficient extraction process and stability evaluation of phycocyanin. BMC chemistry, 15(1): 1-13.
Khazi, M.I., Demirel, Z. and Dalay, M.C. (2018). Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. Journal of applied phycology, 30: 1513-1523.
Kissoudi, M., Sarakatsianos, I. and Samanidou, V. (2018). Isolation and purification of food‐grade C‐phycocyanin from Arthrospira platensis and its determination in confectionery by HPLC with diode array detection. Journal of separation science, 41(4): 975-981.
Kuddus, M., Singh, P., Thomas, G. and Al-Hazimi, A. (2013). Recent developments in production and biotechnological applications of C-phycocyanin. BioMed research international, 2013.
Li, W., Su, H.N., Pu, Y., Chen, J., Liu, L.N., Liu, Q. et al., (2019). Phycobiliproteins: Molecular structure, production, applications, and prospects. Biotechnology Advances, 37(2): 340-353.
Liang, Y., Kaczmarek, M.B., Kasprzak, A.K., Tang, J., Shah, M.M.R., Jin, P. et al., (2018). Thermosynechococcaceae as a source of thermostable C-phycocyanins: Properties and molecular insights. Algal research, 35: 223-235.
Ma, J., Hu, J., Sha, X., Meng, D. and Yang, R. (2022). Phycobiliproteins, the pigment-protein complex form of natural food colorants and bioactive ingredients. Critical Reviews in Food Science and Nutrition, 1-19.
Mandal, M.K., Chanu, N.K. and Chaurasia, N. (2020). Cyanobacterial pigments and their fluorescence characteristics: Applications in research and industry, In: Singh, P.K., Kumar, A., Singh, V.K and Shrivistava, A. (Editors), Advances in Cyanobacterial Biology, 1st Edition, Academic Press, pp. 55-72.
Mysliwa-Kurdziel, B. and Solymosi, K. (2017). Phycobilins and phycobiliproteins used in food industry and medicine. Mini reviews in medicinal chemistry, 17(13): 1173-1193.
Nowruzi, B. (2022). Cyanobacteria Natural Products as Sources for Future Directions in Antibiotic Drug Discovery.
Nowruzi, B., Konur, O. and Anvar, S.A.A. (2022). The stability of the phycobiliproteins in the adverse environmental conditions relevant to the food storage. Food and Bioprocess Technology, 15(12): 2646-2663.
Pagels, F., Guedes, A.C., Amaro, H.M., Kijjoa, A. and Vasconcelos, V. (2019). Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications. Biotechnology Advances, 37(3): 422-443.
Patel, S.N., Sonani, R.R., Roy, D., Singh, N.K., Subudhi, S., Pabbi, S. et al., (2022). Exploring the structural aspects and therapeutic perspectives of cyanobacterial phycobiliproteins. 3 Biotech, 12(9): 224.
Prabakaran, G., Sampathkumar, P., Kavisri, M. and Moovendhan, M. (2020). Extraction and characterization of phycocyanin from Spirulina platensis and evaluation of its anticancer, antidiabetic and antiinflammatory effect. International Journal of Biological Macromolecules, 153: 256-263.
Puzorjov, A., Dunn, K.E. and McCormick, A.J. (2021). Production of thermostable phycocyanin in a mesophilic cyanobacterium. Metabolic engineering communications, 13: e00175.
Puzorjov, A. and McCormick, A.J. (2020). Phycobiliproteins from extreme environments and their potential applications. Journal of Experimental Botany, 71(13): 3827-3842.
Qiang, X., Wang, L., Niu, J., Gong, X. and Wang, G. (2021). Phycobiliprotein as fluorescent probe and photosensitizer: A systematic review. International Journal of Biological Macromolecules, 193: 1910-1917.
Renugadevi, K., Nachiyar, C.V., Sowmiya, P. and Sunkar, S. (2018). Antioxidant activity of phycocyanin pigment extracted from marine filamentous cyanobacteria Geitlerinema sp TRV57. Biocatalysis and agricultural biotechnology, 16: 237-242.
Romay, C.H., Gonzalez, R., Ledon, N., Remirez, D. and Rimbau, V. (2003). C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Current protein and peptide science, 4(3): 207-216.
Safaei, M., Maleki, H., Soleimanpour, H., Norouzy, A., Zahiri, H.S., Vali, H. et al., (2019). Development of a novel method for the purification of C-phycocyanin pigment from a local cyanobacterial strain Limnothrix sp. NS01 and evaluation of its anticancer properties. Scientific reports, 9(1): 9474.
Saini, D.K., Pabbi, S. and Shukla, P. (2018). Cyanobacterial pigments: Perspectives and biotechnological approaches. Food and chemical toxicology, 120: 616-624.
Sauer, P.V., Dominguez-Martin, M.A., Kirst, H., Sutter, M., Bina, D., Greber, B.J. et al., (2021). Structures of the cyanobacterial phycobilisome. BioRxiv, 2021-11.
Sekar, S. and Chandramohan, M. (2008). Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. Journal of Applied Phycology, 20: 113-136.
Shafaei Bejestani, M., Anvar, A.A., Nowruzi, B. and Golestan, L. (2023). Production of cheese and ice cream enriched with biomass and supernatant of Spirulina platensis with emphasis on organoleptic and nutritional properties. Iranian Journal of Veterinary Medicine, DOI: 10.22059/IJVM.2023.355737.1005364
Sharma, R., Nath, P.C., Vanitha, K., Tiwari, O.N., Bandyopadhyay, T.K. and Bhunia, B. (2021). Effects of different monosaccharides on thermal stability of phycobiliproteins from Oscillatoria sp. (BTA-170): Analysis of kinetics, thermodynamics, colour and antioxidant properties. Food Bioscience, 44: 101354.
Vinothkanna, A. and Sekar, S. (2020). Diagnostic Applications of Phycobiliproteins. Pigments from Microalgae Handbook, 585-610.
Yuan, B., Zhuxin, L., Honghong, S., Dashnyam, B., Xiao, X., McClements, D.J., et al., (2022). A review of recent strategies to improve the physical stability of phycocyanin. Current Research in Food Science, 5: 2329-2337.
Zuorro, A., Leal-Jerez, A.G., Morales-Rivas, L.K., Mogollón-Londoño, S.O., Sanchez-Galvis, E.M., García-Martínez, J.B. et al., (2021). Enhancement of Phycobiliprotein Accumulation in Thermotolerant Oscillatoria sp. through Media Optimization. ACS omega, 6(16): 10527-10536.
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