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Kumari Neha, Jaiswal Jyoti, Gupta Amit, Singh Varsha K., Sinha Rajeshwar P.
Keywords: Antioxidant activity, Cyanobacteria, Nuclear magnetic resonance (NMR) spectroscopy, n Scytonema sp. HKAR-8, Scytonemin
The most promising class of photosynthetic microorganisms, cyanobacteria, can produce a wide range of useful natural products. Some cyanobacteria are capable of biosynthesizing the indole-alkaloid scytonemin, a secondary metabolite of significant ecological and medicinal value. Scytonemin is a small, yellow-brown, 544-Da molecular mass, lipid-soluble compound that can screen UV-A radiation. In this study, scytonemin was extracted and purified from the cyanobacterium Scytonema sp. HKAR-8. Further, nuclear magnetic resonance (NMR) spectroscopy was used to identify and characterize scytonemin. The antioxidant potentials of scytonemin were assessed using several in vitro antioxidant tests, including DPPH, ABTS, and H2O2 scavenging activity. Scytonemin extracted from this cyanobacterium showed dose-dependent in vitro antioxidant activity as compared to ascorbic acid. By producing the photoprotective compound scytonemin, cyanobacteria can colonize and thrive in harsh environmental conditions by reducing the negative effects of UV radiation. This UV-shielding compound, scytonemin may be of significant importance for the formation of natural and sustainable sunscreen in the cosmetic and other therapeutic industries because of its significant antioxidant capacity and photoprotective activity.
Arnao M, Cano A, Hernandez-Ruiz J, Garcia-Cánovas F, Acosta M (1996) Inhibition by L-ascorbic acid and other antioxidants of the 2,2′-azino-bis (3-ethylbenzthiazoline-6-sulfonic Acid) oxidation catalyzed by peroxidase: a new approach for determining total antioxidant status of foods. Anal Biochem 236:255–261. https://doi.org/10.1006/abio.1996.0164
Bultel-Poncé V, Félix-Théodose F, Sarthou C, Ponge JF, Bodo B (2004) New pigments from the terrestrial Cyanobacterium Scytonema sp. collected on the Mitaraka inselberg, French Guyana. J Nat Prod 67(4):678–681. https://doi.org/10.1021/np034031u
Couradeau E, Karaoz U, Lim HC, Da Rocha UN, Northen T, Brodie E, Garcia-Pichel F (2016) Bacteria increase arid-land soil surface temperature through the production of sunscreens. Nat Commun 7:1–7. https://doi.org/10.1038/ncomms10373
Casero MC, Ascaso C, Quesada A, Mazur-Marzec H, Wierzchos J (2021) Response of endolithic Chroococcidiopsis strains from the polyextreme Atacama desert to light radiation. Front Microbiol 11:614875. https://doi.org/10.3389/fmicb.2020.614875
Chaiklahan R, Chirasuwan N, Triratana P, Loha V, Tia S, Bunnag B (2013) Polysaccharide extraction from Spirulina sp. and its antioxidant capacity. Int J Biol Macromol 58:73–78. https://doi.org/10.1016/j.ijbiomac.2013.03.046
Dillon JG, Castenholz RW (1999) Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. J Phycol 35:673–681. https://doi.org/10.1046/j.1529-8817.1999.3540673.x
Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a Cyanobacterium (Chroococcidiopsis sp). Arch Microbiol 177:322–331
Dillon JG, Castenholz RW (2003) The synthesis of the UV-screening pigment, scytonemin, and photosynthetic performance in isolates from closely related natural populations of cyanobacteria (Calothrix sp). Environ Microbiol 5:484–491. https://doi.org/10.1046/j.1462-2920.2003.00436.x
Evans J, Jones A, Blumenthal E, Soule T (2021) Anti-proliferation of melanoma cells and immune stimulation by the cyanobacterial indole-alkaloid scytonemin. Fine Focus 7:54–63. https://doi.org/10.33043/FF.7.1.54-63
Fleming ED, Castenholz RW (2007) Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environ Microbiol 9:1448–1455. https://doi.org/10.1111/j.1462-2920.2007.01261.x
Fleming ED, Castenholz RW (2008) Effects of nitrogen source on the synthesis of the UV screening compound, scytonemin, in the Cyanobacterium Nostoc punctiforme PCC 73102. FEMS Microbiol Ecol 63:301–308. https://doi.org/10.1111/j.1574-6941.2007.00432.x
Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9:791–802. https://doi.org/10.1038/nrmicro2649
Gao X, Jing X, Liu X, Lindblad P (2021) Biotechnological production of the sunscreen pigment scytonemin in cyanobacteria: progress and strategy. Mar Drugs 19:129. https://doi.org/10.3390/md19030129
Garcia-Pichel F, Castenholz RW (1991) Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J Phycol 27:395–409. https://doi.org/10.1111/j.0022-3646.199100395.x
Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169. https://doi.org/10.1128/aem.59.1.163-169.1993
Garcia-Pichel F, Wingard CE, Castenholz RW (1993) Evidence regarding the UV sunscreen role of a mycosporine-like compound in the Cyanobacterium Gloeocapsa Sp. Appl Environ Microbiol 59:170–176. https://doi.org/10.1128/aem.59.1.170-176.1993
Gupta A, Singh AP, Singh V, Singh PR, Jaiswal J, Kumari N, Upadhye V, Singh SC, Sinha RP (2023) Natural Sun-screening compounds and DNA-repair enzymes: photoprotection and photoaging. Catalysts 13:1–23. https://doi.org/10.3390/catal13040745
Häder D-P, Williamson CE, Wängberg S-A, Rautio M, Rose KC, Gao K, Helbling EW, Sinha RP, Worrest R (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14:108–126. https://doi.org/10.1039/C4PP90035A
Häder DP, Kumar HD, Smith RC, Worrest RC (1998) Effects on aquatic ecosystems. J Photochem Photobiol B Biol 46:53–68. https://doi.org/10.1016/S1011-1344(98)00185-7
Hunsucker SW, Tissue BM, Potts M, Helm RF (2001) Screening protocol for the ultraviolet-photoprotective pigment scytonemin. Anal Biochem 288:227–230. https://doi.org/10.1006/abio.2000.4895
Kaur H, Perkins J (1991) The free radical chemistry of food additives. In: Halliwell B (ed) Free radicals and food additives. Taylor & Francis Ltd., London, pp 17–35
Keser S, Celik S, Turkoglu S (2013) Total phenolic contents and free-radical scavenging activities of grape (Vitis vinifera L.) and grape products. Int J Food Sci Nutr 64(2):210–216. https://doi.org/10.3109/09637486.2012.728199
Kumari N, Pandey A, Gupta A, Mishra S, Sinha RP (2023) Characterization of UV-screening pigment scytonemin from cyanobacteria inhabiting diverse habitats of varanasi, India. Biologia 78(2):319–330. https://doi.org/10.1007/s11756-022-01190-9
Kumari N, Pathak J, Dwivedy AK, Sinha RP (2021) Bioprospection of UV-screening compounds from lichens inhabiting the Indian state of Sikkim. Plant Arch 21:1168–1177. https://doi.org/10.51470/PLANTARCHIVES.2021.v21.no1.155
Matsui K, Nazif E, Hirai Y, Wada N, Matsugo S, Sakamoto T (2012) The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. J Gen Appl Microbiol 58:137–144. https://doi.org/10.2323/jgam.58.137
Miller NJ, Rice-Evans C (1997) Factor influencing the antioxidant activity determined by the ABTS + radical cation assay. Free Radic Res 26:195–199. https://doi.org/10.3109/1071576970
Morone J, Alfeus A, Vasconcelos V, Martins R (2019) Revealing the potential of cyanobacteria in cosmetics and cosmeceuticals-a new bioactive approach. Algal Res 41:101541. https://doi.org/10.1016/j.algal.2019.101541
Naeimpoor F, Sheibani Madrahi G (2022) UV induced biosynthesis of Cyano-sunscreen scytonemin by Leptolyngbya mycodia and its effectual antioxidant activity. Iran J Pharm Sci 18(1):19–33
Němečková K, Culka A, Němec I, Edwards HG, Mareš J, Jehlička J (2021) Raman spectroscopic search for scytonemin and gloeocapsin in endolithic colonizations in large gypsum crystals. J Raman Spectrosc 52:2633–2647. https://doi.org/10.1002/jrs.6186
Pandey A, Kumari N, Mishra S, Jaiswal J, Sinha RP (2022) NMR spectroscopy for the characterization of photoprotective compounds in cyanobacteria. In: Rahman A, Choudhary MI (eds) Applications of NMR spectroscopy, Bentham science publishers. Pte. Ltd., Singapore, pp 1–34
Pandey A, Pathak J, Singh DK, Ahmed H, Singh V, Kumar D, Sinha RP (2020) Photoprotective role of UV-screening pigment scytonemin against UV-B-induced damages in the heterocyst-forming Cyanobacterium Nostoc sp. strain HKAR-2. Brazilian J Bot 43:67–80. https://doi.org/10.1007/s40415-020-00589-5
Pathak J, Sonker AS, Kannaujiya VK, Singh V, Ahmed H, Sinha RP (2017) Screening and partial purification of photoprotective pigment scytonemin from cyanobacterial crusts dwelling on the historical monuments in and around Varanasi, India. Microbiol Res 8:6559. https://doi.org/10.4081/mr.2017.6559
Pathak J, Kumar D, Singh DK, Ahmed H, Kannaujiya VK, Sinha RP (2022) Ultraviolet radiation and salinity-induced physiological changes and scytonemin induction in cyanobacteria isolated from diverse habitats. Biointerface Res Appl Chem 12:3590–3606. https://doi.org/10.33263/BRIAC123.35903606
Proteau PJ, Gerwick WH, Garcia-Pichel F, Castenholz R (1993) The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49:825–829. https://doi.org/10.1007/BF01923559
Rastogi RP, Sinha RP, Incharoensakdi A (2013) Partial characterization, UV-induction and photoprotective function of sunscreen pigment, scytonemin from Rivularia sp. HKAR-4. Chemosphere 93:1874–1878. https://doi.org/10.1016/j.chemosphere.2013.06
Rastogi RP, Sonani RR, Madamwar D, Incharoensakdi A (2016) Characterization and antioxidant functions of mycosporine-like amino acids in the Cyanobacterium Nostoc sp. R76DM. Algal Res 16:110–118. https://doi.org/10.1016/j.algal.2016.03.009
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237. https://doi.org/10.1016/S0891-5849(98)00315-3
Ruch RJ, Cheng SJ, Klaunig JE (1989) Prevention of cytotoxicity and Inhibition of intracellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10:1003–1008. https://doi.org/10.1093/carcin/10.6.1003
Sen S, Mallick N (2022) Scytonemin: unravelling major progress and prospects. Algal Res 64:102678. https://doi.org/10.1016/j.algal.2022.102678
Sharma S, Sharma RK, Gaur K, Cátala Torres JF, Loza-Rosas SA, Torres A, Saxena M, Julin M, Tinoco AD (2019) Fueling a hot debate on the application of TiO2 nanoparticles in sunscreen. Materials 12:2317. https://doi.org/10.3390/ma12142317
Singh G, Babele PK, Sinha RP, Tyagi MB, Kumar A (2013a) Enzymatic and non-enzymatic defense mechanisms against ultraviolet-B radiation in two Anabaena species. Process Biochem 48:796–802. https://doi.org/10.1016/j.procbio.2013.04.022
Singh SP, Rastogi RP, Sinha RP, Häder D-P (2013b) Photosynthetic performance of Anabaena variabilis PCC 7937 under simulated solar radiation. Photosynthetica 51:259–266. https://doi.org/10.1007/s11099-013-0012-7
Sinha RP, Häder D-P (2008) UV-protectants in cyanobacteria. Plant Sci 174:278–289. https://doi.org/10.1016/j.plantsci.2007.12.004
Stevenson CS, Capper EA, Roshak AK, Marquez B, Eichman C, Jackson JR, Mattern M, Gerwick WH, Jacobs RS, Marshall LA (2002a) The identification and characterization of the marine natural product scytonemin as a novel antiproliferative pharmacophore. J Pharmacol Exp Ther 303:858–866. https://doi.org/10.1124/jpet.102.036350
Stevenson CS, Capper EA, Roshak AK, Marquez B, Grace K, Gerwick WH, Jacobs RS, Marshall LA (2002b) Scytonemin-a marine natural product inhibitor of kinases key in hyperproliferative inflammatory diseases. Infamm Res 51:112–114. https://doi.org/10.1007/BF02684014
Valentao P, Fernandes E, Carvalho F, Andrade PB, Seabra RM, Bastos ML (2002) Antioxidative properties of cardoon (Cynara cardunculus L.) infusion against superoxide radical hydroxyl radical, and hypochlorous acid. J Agri Food Chem 50:4989–4993. https://doi.org/10.1021/jf020225o
Vincent WF, Roy S (1993) Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery. Environ Rev 1:1–12. https://doi.org/10.1139/a93-00
Wright DJ, Smith SC, Joardar V, Scherer S, Jervis J, Warren A, Helm RF, Potts M (2005) UV irradiation and desiccation modulate the three-dimensional extracellular matrix of Nostoc commune (Cyanobacteria). J Biol Chem 40271–40281. https://doi.org/10.1074/jbc.M505961200
Zheng W, Wang SY (2001) Antioxidant activity and phenolic compounds in selected herbs. J Agri Food Chem 49:5165–5170. https://doi.org/10.1021/jf010697n
Laboratory of Photobiology and Molecular Microbiology, Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, India