Chemical characterization and antioxidant activity of raw extract of photosynthesizing microorganisms from the Chapada das Mesas National Park Brazilian Cerrado
DOI:
https://doi.org/10.5281/zenodo.20766092Palavras-chave:
Bioprospecting, Chlorella, Nostoc, Synechococcus, Secondary metabolitesResumo
Cyanobacteria and microalgae are photosynthetic microorganisms that produce bioactive compounds such as carotenoids, flavonoids, and fatty acids, which are of importance to the pharmaceutical, cosmetic, food, and biofuels industries. This study aimed to investigate the bioactive potential of extracts from the microalgae Chlorella sp. (GBBB06) and the cyanobacteria Nostoc sp. (GBBB01) and Synechococcus sp. (GBBB07), collected in the Chapada das Mesas National Park, Cerrado Maranhense. Methanolic extracts of the samples were obtained to chemically characterize them using chromatographic techniques, such as thin-layer chromatography, high performance liquid chromatography coupled with a diode arrangement detector, and gas chromatography coupled to mass spectrometry. To evaluate the antioxidant capacity, DPPH• and ABTS•+ assays were performed. Were found on liquid chromatography, peaks with characteristic wavelengths of carotenoids in the sample of Chlorella sp. and those characteristic of chlorophyll in all samples. Metabolites such as fatty acids, alcohols, and nitrogen compounds were identified via gas chromatography. In the antioxidant assessment, the samples scavenged 12% (Nostoc sp.), 20% (Chlorella sp.), and 25% (Synechococcus sp.) of the radical DPPH• in extract concentrations of 0.675 mg/mL. The results for ABTS•+ radical assay showed high antioxidant potential in the samples, with scavenging of 60% (Chlorella sp.) and 70% (Synechococcus sp. and Nostoc sp.). These results demonstrated that Chlorella sp., Nostoc sp., and Synechococcus sp. are rich in bioactive secondary metabolites with antioxidant properties and potential biotechnological applications; these extracts represent an alternative for economic exploitation of the Brazilian Cerrado in a sustainable manner.
Referências
ABOIM, Joseline Barbosa et al. Determination of biodiesel properties based on a fatty acid profile of eight Amazon cyanobacterial strains grown in two different culture media. RSC Advances, v. 6, n. 111, p. 109751–109758, 2016. Disponível em: https://doi.org/10.1039/C6RA23268J.
ADAMAKIS, Ioannis-Dimosthenis et al. Cultivation, characterization, and properties of Chlorella vulgaris microalgae with different lipid contents and effect on fast pyrolysis oil composition. Environmental Science and Pollution Research, v. 25, 2018. Disponível em: https://doi.org/10.1007/s11356-018-2368-5.
AMARO, Helena M.; GUEDES, A. Catarina; MALCATA, F. Xavier. Advances and perspectives in using microalgae to produce biodiesel. Applied Energy, v. 88, 2011. Disponível em: https://doi.org/10.1016/J.APENERGY.2010.12.014.
AMRANI-ALLALOU, Hanane et al. Antioxidant activity, carotenoids, chlorophylls and mineral composition from leaves of Pallenis spinosa: an Algerian medicinal plant. Journal of Complementary and Integrative Medicine, v. 17, n. 1, 2019. Disponível em: https://doi.org/10.1515/jcim-2017-0081.
ANANYA; KAMAL, Aisha. Fatty acid profiling and antioxidant potential of total polar lipid content of cyanobacterium Nostoc muscurum. International Journal of Pharmacy and Pharmaceutical Sciences, p. 159–163, 2016.
BAJPAI, Vivek K. et al. Developments of cyanobacteria for nano-marine drugs: relevance of nanoformulations in cancer therapies. Marine Drugs, v. 16, n. 6, p. 179, 2018. Disponível em: https://doi.org/10.3390/md16060179.
DANDEKAR, Rucha; FEGADE, Bharti; VH, Bhaskar. GC-MS analysis of phytoconstituents in alcohol extract of Epiphyllum oxypetalum leaves. Journal of Pharmacognosy and Phytochemistry, 2015.
DEMAY, Justine et al. Natural products from cyanobacteria: focus on beneficial activities. Marine Drugs, v. 17, n. 6, p. 320, 2019. Disponível em: https://doi.org/10.3390/md17060320.
DITTMANN, Elke et al. Natural product biosynthetic diversity and comparative genomics of the cyanobacteria. Trends in Microbiology, v. 23, n. 10, p. 642–652, 2015. Disponível em: https://doi.org/10.1016/j.tim.2015.07.008.
FARROKH, Parisa et al. Cyanobacteria as an eco-friendly resource for biofuel production: a critical review. Biotechnology Progress, v. 35, n. 5, e2835, 2019. Disponível em: https://doi.org/10.1002/btpr.2835.
FERRUZZI, Mario G.; BLAKESLEE, Joshua. Digestion, absorption, and cancer preventative activity of dietary chlorophyll derivatives. Nutrition Research, v. 27, n. 1, p. 1–12, 2007. Disponível em: https://doi.org/10.1016/j.nutres.2006.12.003.
HASHTROUDI, Mehri Seyed et al. Analysis of Anabaena vaginicola and Nostoc calcicola from Northern Iran, as rich sources of major carotenoids. Food Chemistry, v. 136, n. 3, p. 1148–1153, 2013. Disponível em: https://doi.org/10.1016/j.foodchem.2012.09.055.
HASSAN, Saqib et al. Identification and characterization of the novel bioactive compounds from microalgae and cyanobacteria for pharmaceutical and nutraceutical applications. Journal of Basic Microbiology, v. 62, n. 9, p. 999–1029, 2022. Disponível em: https://doi.org/10.1002/jobm.202100477.
HEMALATHA, Annadurai et al. Antioxidant properties and total phenolic content of a marine diatom, Navicula clavata and green microalgae, Chlorella marina and Dunaliella salina. Advances in Applied Science Research, v. 4, p. 151–157, 2013.
HU, Jianjun et al. Heterotrophic cultivation of microalgae for pigment production: a review. Biotechnology Advances, v. 36, n. 1, p. 54–67, 2018. Disponível em: https://doi.org/10.1016/j.biotechadv.2017.09.009.
ISLAM, Muhammad Torequl et al. Phytol: a review of biomedical activities. Food and Chemical Toxicology, v. 121, p. 82–94, 2018. Disponível em: https://doi.org/10.1016/j.fct.2018.08.032.
JEREZ-MARTEL, Idaira et al. Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains. Journal of Food Quality, v. 2017, p. 2924508, 2017. Disponível em: https://doi.org/10.1155/2017/2924508.
KAMFFER, Zindi; BINDON, Keren; OBERHOLSTER, A. Optimization of a method for the extraction and quantification of carotenoids and chlorophylls during ripening in grape berries (Vitis vinifera cv. Merlot). Journal of Agricultural and Food Chemistry, v. 58, p. 6578–6586, 2010. Disponível em: https://doi.org/10.1021/jf1004308.
KHOEYI, Zahra; SEYFABADI, Jafar; RAMEZANPOUR, Zohreh. Effect of light intensity and photoperiod on biomass and fatty acid composition of the microalgae Chlorella vulgaris. Aquaculture International, v. 20, 2012. Disponível em: https://doi.org/10.1007/s10499-011-9440-1.
KOBAYASHI, Naoko et al. Rapid detection and quantification of triacylglycerol by HPLC-ELSD in Chlamydomonas reinhardtii and Chlorella strains. Lipids, v. 48, n. 10, p. 1035–1049, 2013. Disponível em: https://doi.org/10.1007/s11745-013-3828-9.
KOMÁREK, Jiří. Recent changes (2008) in cyanobacteria taxonomy based on a combination of molecular background with phenotype and ecological consequences (genus and species concept). Hydrobiologia, v. 639, n. 1, p. 245–259, 2010. Disponível em: https://doi.org/10.1007/s10750-009-0031-3.
LEE, Jay et al. Natural products and body weight control. North American Journal of Medical Sciences, v. 3, n. 1, p. 13–19, 2011. Disponível em: https://doi.org/10.4297/najms.2011.313.
LEKSHMI, S.; SARAMMA, A. V. Antioxidant activity of Synechococcus sp. Nägeli isolated from Cochin estuary, India. Indian Journal of Geo-Marine Sciences, v. 47, p. 2213–2216, 2018.
LÜTKE-BRINKHAUS, F.; WEISS, G.; KLEINIG, H. Prenyl lipid formation in spinach chloroplasts and in a cell-free system of Synechococcus (Cyanobacteria): polyprenols, chlorophylls, and fatty acid prenyl esters. Planta, v. 163, n. 1, p. 68–74, 1985. Disponível em: https://doi.org/10.1007/BF00395899.
MARTINS, Teresa; ARSIN, Sila; FEWER, David; LEÃO, Pedro. UV-protective secondary metabolites from cyanobacteria. In: Cyanobacteria. [S.l.]: Academic Press, 2022. p. 107–144. Disponível em: https://doi.org/10.1016/B978-0-12-821491-6.00005-3.
MEZZOMO, Natália; FERREIRA, Sandra R. S. Carotenoids functionality, sources, and processing by supercritical technology: a review. Journal of Chemistry, v. 2016, p. 3164312, 2016. Disponível em: https://doi.org/10.1155/2016/3164312.
MUYS, Maarten et al. High variability in nutritional value and safety of commercially available Chlorella and Spirulina biomass indicates the need for smart production strategies. Bioresource Technology, v. 275, p. 247–257, 2019. Disponível em: https://doi.org/10.1016/j.biortech.2018.12.059.
NIEDERMEYER, Timo Horst Johannes. Anti-infective natural products from cyanobacteria. Planta Medica, v. 81, n. 15, p. 1309–1325, 2015. Disponível em: https://doi.org/10.1055/s-0035-1546055.
NOZZI, Nicole E.; OLIVER, John W. K.; ATSUMI, Shota. Cyanobacteria as a platform for biofuel production. Frontiers in Bioengineering and Biotechnology, v. 1, 2013. Disponível em: https://doi.org/10.3389/fbioe.2013.00007.
OBULESU, M.; DOWLATHABAD, Muralidhara Rao; BRAMHACHARI, P. V. Carotenoids and Alzheimer’s disease: an insight into therapeutic role of retinoids in animal models. Neurochemistry International, v. 59, n. 5, p. 535–541, 2011. Disponível em: https://doi.org/10.1016/j.neuint.2011.04.004.
OZAWA, Yoko et al. Neuroprotective effects of lutein in the retina. Current Pharmaceutical Design, v. 18, n. 1, p. 51–56, 2012. Disponível em: https://doi.org/10.2174/138161212798919101.
PARK, Jean Soon et al. Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutrition & Metabolism, v. 7, p. 18, 2010. Disponível em: https://doi.org/10.1186/1743-7075-7-18.
PARMAR, Asha et al. Retracted: Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresource Technology, v. 102, n. 22, p. 10163–10172, 2011. Disponível em: https://doi.org/10.1016/j.biortech.2011.08.030.
PATIAS, Luciana D. et al. Carotenoid profile of three microalgae/cyanobacteria species with peroxyl radical scavenger capacity. Food Research International, v. 100, pt. 1, p. 260–266, 2017. Disponível em: https://doi.org/10.1016/j.foodres.2017.06.069.
PLAZA, Merichel et al. Comprehensive characterization of the functional activities of pressurized liquid and ultrasound-assisted extracts from Chlorella vulgaris. LWT – Food Science and Technology, v. 46, p. 245–253, 2012. Disponível em: https://doi.org/10.1016/j.lwt.2011.09.024.
PRIYADARSHANI, Indira; RATH, Biswajit. Commercial and industrial applications of micro algae: a review. Journal of Algal Biomass Utilization, v. 3, n. 4, p. 89–100, 2012.
RAJA, R.; HEMAISWARYA, S.; RENGASAMY, R. Exploitation of Dunaliella for beta-carotene production. Applied Microbiology and Biotechnology, v. 74, n. 3, p. 517–523, 2007. Disponível em: https://doi.org/10.1007/s00253-006-0777-8.
RAJESWARI, Gopalasamy; MURUGAN, M.; MOHAN, Veerabahu. GC-MS analysis of bioactive components of Hugonia mystax L. (Linaceae). Research Journal of Pharmaceutical, Biological and Chemical Sciences, v. 3, p. 301–308, 2012.
RASTOGI, Rajesh P.; SINHA, Rajeshwar P. Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnology Advances, v. 27, n. 4, p. 521–539, 2009. Disponível em: https://doi.org/10.1016/j.biotechadv.2009.04.009.
RIBEIRO, Eliana Paula; SERAVALLI, Elisena A. G. Química de alimentos. São Paulo: Blucher, 2007.
RIBEIRO, Michele et al. Antiviral activity of microalgae extracts against Mayaro virus. Algal Research, v. 61, p. 102577, 2022. Disponível em: https://doi.org/10.1016/j.algal.2021.102577.
RICHA; SINHA, Rajeshwar P. Biochemical characterization of sunscreening mycosporine-like amino acids from two Nostoc species inhabiting diverse habitats. Protoplasma, v. 252, n. 1, p. 199–208, 2015. Disponível em: https://doi.org/10.1007/s00709-014-0674-4.
RODRIGUES, Daniele B. et al. Production of carotenoids from microalgae cultivated using agroindustrial wastes. Food Research International, v. 65, p. 144–148, 2014. Disponível em: https://doi.org/10.1016/j.foodres.2014.06.037.
RODRIGUES, Daniele B. et al. Bioactive pigments from microalgae Phormidium autumnale. Food Research International, v. 77, p. 273–279, 2015. Disponível em: https://doi.org/10.1016/j.foodres.2015.04.027.
ROMERO-LOPEZ, Julia; LOPEZ-RODAS, Victoria; COSTAS, Eduardo. Estimating the capability of microalgae to physiological acclimatization and genetic adaptation to petroleum and diesel oil contamination. Aquatic Toxicology, v. 124–125, p. 227–237, 2012. Disponível em: https://doi.org/10.1016/j.aquatox.2012.08.001.
RYU, Sung Kee et al. Effect of an oral astaxanthin prodrug (CDX-085) on lipoprotein levels and progression of atherosclerosis in LDLR(-/-) and ApoE(-/-) mice. Atherosclerosis, v. 222, n. 1, p. 99–105, 2012. Disponível em: https://doi.org/10.1016/j.atherosclerosis.2012.02.002.
SÁNCHEZ-MORENO, Concepción; LARRAURI, José A.; SAURA-CALIXTO, Fulgencio. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture, v. 76, n. 2, p. 270–276, 1998. Disponível em: https://doi.org/10.1002/(SICI)1097-0010(199802)76:2<270::AID-JSFA945>3.0.CO;2-9.
SALEM, Olfat et al. Antimicrobial activity of microalgal extracts with special emphasize on Nostoc sp. Life Science Journal, v. 11, p. 752–758, 2014.
SCHOEFS, Benoît. Chlorophyll and carotenoid analysis in food products: properties of the pigments and methods of analysis. Trends in Food Science & Technology, v. 13, n. 11, p. 361–371, 2002. Disponível em: https://doi.org/10.1016/S0924-2244(02)00182-6.
SHANAB, Sanaa M. M. et al. Aqueous extracts of microalgae exhibit antioxidant and anticancer activities. Asian Pacific Journal of Tropical Biomedicine, v. 2, n. 8, p. 608–615, 2012. Disponível em: https://doi.org/10.1016/S2221-1691(12)60106-3.
STINCO, Carla M. et al. Development and validation of a rapid resolution liquid chromatography method for the screening of dietary plant isoprenoids: carotenoids, tocopherols and chlorophylls. Journal of Chromatography A, v. 1370, p. 162–170, 2014. Disponível em: https://doi.org/10.1016/j.chroma.2014.10.044.
TUMOLO, Tathyana; LANFER-MARQUEZ, Ursula Maria. Copper chlorophyllin: a food colorant with bioactive properties? Food Research International, v. 46, n. 2, p. 451–459, 2012. Disponível em: https://doi.org/10.1016/j.foodres.2011.10.031.
VALDUGA, Eunice et al. Carotenoids production: microorganisms as source of natural dyes. Química Nova, v. 32, p. 2429–2436, 2009. Disponível em: https://doi.org/10.1590/S0100-40422009000900036.
VALENTE, Ligia M. M. et al. Development and application of a thin layer chromatographic method for the determination of the pentacyclic oxindole alkaloid profile in South American species of the genus Uncaria. Revista Brasileira de Farmacognosia, v. 16, p. 216–223, 2006. Disponível em: https://doi.org/10.1590/S0102-695X2006000200015.
VERMA, E.; SINGH, S.; NIVESHIKA; MISHRA, A. K. Salinity-induced oxidative stress-mediated change in fatty acids composition of cyanobacterium Synechococcus sp. PCC7942. Journal of Environmental Science and Pollution Research, v. 16, n. 2, p. 875–886, 2019. Disponível em: https://doi.org/10.1007/s13762-018-1720-0.
VERMA, Narendra et al. Prospective of biodiesel production utilizing microalgae as the cell factories: a comprehensive discussion. African Journal of Biotechnology, v. 9, p. 1402–1411, 2010. Disponível em: https://doi.org/10.5897/AJBx09.071.
VOLP, Ana; RENHE, Isis; STRINGHETA, Paulo. Pigmentos naturais bioativos. Alimentos e Nutrição, v. 20, 2009.
WIDIYANTO, Slamet et al. Biochemical compounds and sub-chronic toxicity test of Chlorella sp. and Spirulina sp. isolated from Glagah Coastal Water. Berkala Penelitian Hayati, v. 24, p. 58–64, 2018. Disponível em: https://doi.org/10.23869/bphjbr.24.1.20189.
WINNIKOFF, Jacob R. et al. Quantitative molecular networking to profile marine cyanobacterial metabolomes. The Journal of Antibiotics, v. 67, n. 1, p. 105–112, 2014. Disponível em: https://doi.org/10.1038/ja.2013.120.
YOUNG, Andrew J.; LOWE, Gordon L. Carotenoids: antioxidant properties. Antioxidants, v. 7, n. 2, p. 28, 2018. Disponível em: https://doi.org/10.3390/antiox7020028.
YUCHAROEN, Raenu; SRISUKSOMWONG, Pawalee; TRAGOOLPUA, Yingmanee. Antibacterial and antioxidant activities of Nostoc commune Vaucher ex Bornet & Flahault. Progress in Applied Science and Technology, v. 5, n. 2, p. 35–48, 2015.
ZHANG, Jie et al. Microalgal carotenoids: beneficial effects and potential in human health. Food & Function, v. 5, n. 3, p. 413–425, 2014. Disponível em: https://doi.org/10.1039/c3fo60607d.



































