Antioxidant profiling of cyanobacterial bioactive compounds
DOI:
https://doi.org/10.18686/fnc254Keywords:
antioxidants; cosmeceuticals; cyanobacteria; cyanolichens; nutraceuticalsAbstract
Antioxidant compounds may be useful as dietary supplements that protect from oxidative-stress-related diseases. Different organisms produce antioxidants as a defense mechanism to counteract the damaging effects of free radicals. Reactive oxygen species, reactive nitrogen species, and even chloride ions are harmful to living systems. Cyanobacteria produce a wide range of bioactive compounds with diverse applications in agriculture, medicine, and industry. These compounds include pigments and secondary metabolites, such as mycosporine-like amino acids, scytonemin, carotenoids, phycobiliproteins, and other molecules with antioxidant and anti-inflammatory properties. The antioxidant molecules found in cyanobacteria may provide a safe, natural, and alternative substitute for synthetic antioxidants. They may also find an application in nutraceuticals and cosmeceuticals. The antioxidant properties of cyanobacteria are ecologically significant, enabling their survival and resilience in extreme environments. Important advancements in the field of antioxidants derived from cyanobacteria are highlighted in this review. The novelty of this review lies in the fact that it emphasizes cyanobacteria as sustainable and renewable resources for natural antioxidants for reducing dependency on synthetic chemicals. A sustainable method of envisaging cyanobacteria as competent antioxidants may lead to new developments in the fields of diagnosis, management, and prevention of a wide range of diseases. This study also emphasizes the ecological and industrial relevance of cyanobacteria as sustainable sources of bioactive compounds for addressing oxidative-stress-related challenges.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Varsha K. Singh, Sapana Jha, Palak Rana, Riya Tripathi, Ashish P. Singh, Rajeshwar P. Sinha

This work is licensed under a Creative Commons Attribution 4.0 International License.
References
1. Cervantes Gracia K, Llanas-Cornejo D, Husi H. CVD and Oxidative Stress. Journal of Clinical Medicine. 2017; 6(2): 22. doi: 10.3390/jcm6020022
2. Mishra S, Kumari N, Singh VK, et al. Cyanobacterial Biofuel: A Platform for Green Energy. Advances in Environmental and Engineering Research. 2023; 04(03): 1-42. doi: 10.21926/aeer.2303041
3. Singh VK, Jha S, Rana P, et al. Cyanobacteria as a Biocatalyst for Sustainable Production of Biofuels and Chemicals. Energies. 2024; 17(2): 408. doi: 10.3390/en17020408
4. Sies H. Oxidative Stress: Concept and Some Practical Aspects. Antioxidants. 2020; 9(9): 852. doi: 10.3390/antiox9090852
5. Janknegt PJ, Van De Poll WH, Visser RJW, et al. Oxidative stress responses in the marine Antarctic diatom Chaetoceros brevis (Bacillariophyceae) during photoacclimation1. Journal of Phycology. 2008; 44(4): 957-966. doi: 10.1111/j.1529-8817.2008.00553.x
6. Singh VK, Das B, Jha S, et al. Characterization, DFT study and evaluation of antioxidant potentials of mycosporine-like amino acids (MAAs) in the cyanobacterium Anabaenopsis circularis HKAR-22. Journal of Photochemistry and Photobiology B: Biology. 2024; 257: 112975. doi: 10.1016/j.jphotobiol.2024.112975
7. Rai R, Singh S, Rai KK, et al. Regulation of antioxidant defense and glyoxalase systems in cyanobacteria. Plant Physiology and Biochemistry. 2021; 168: 353-372. doi: 10.1016/j.plaphy.2021.09.037
8. Morone J, Alfeus A, Vasconcelos V, et al. Revealing the potential of cyanobacteria in cosmetics and cosmeceuticals — A new bioactive approach. Algal Research. 2019; 41: 101541. doi: 10.1016/j.algal.2019.101541
9. Singh DP, Prabha R, Verma S, et al. Antioxidant properties and polyphenolic content in terrestrial cyanobacteria. 3 Biotech. 2017; 7(2). doi: 10.1007/s13205-017-0786-6
10. Wada N, Sakamoto T, Matsugo S. Mycosporine-Like Amino Acids and Their Derivatives as Natural Antioxidants. Antioxidants. 2015; 4(3): 603-646. doi: 10.3390/antiox4030603
11. Jerez-Martel I, García-Poza S, Rodríguez-Martel G, et al. Phenolic Profile and Antioxidant Activity of Crude Extracts from Microalgae and Cyanobacteria Strains. Journal of Food Quality. 2017; 2017: 1-8. doi: 10.1155/2017/2924508
12. Guerreiro A, Andrade MA, Menezes C, et al. Antioxidant and Cytoprotective Properties of Cyanobacteria: Potential for Biotechnological Applications. Toxins. 2020; 12(9): 548. doi: 10.3390/toxins12090548
13. Ijaz S, Hasnain S. Antioxidant potential of indigenous cyanobacterial strains in relation with their phenolic and flavonoid contents. Natural Product Research. 2015; 30(11): 1297-1300. doi: 10.1080/14786419.2015.1053088
14. Shick JM, Dunlap WC. Mycosporine-Like Amino Acids and Related Gadusols: Biosynthesis, Accumulation, and UV-Protective Functions in Aquatic Organisms. Annual Review of Physiology. 2002; 64(1): 223-262. doi: 10.1146/annurev.physiol.64.081501.155802
15. Singh VK, Jha S, Rana P, et al. Application of Synthetic Biology Approaches to High-Yield Production of Mycosporine-like Amino Acids. Fermentation. 2023; 9(7): 669. doi: 10.3390/fermentation9070669
16. Matsui K, Nazifi E, Hirai Y, et al. The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. The Journal of General and Applied Microbiology. 2012; 58(2): 137-144. doi: 10.2323/jgam.58.137
17. Rastogi RP, Incharoensakdi A. Characterization of UV-screening compounds, mycosporine-like amino acids, and scytonemin in the cyanobacterium Lyngbya sp. CU2555. FEMS Microbiology Ecology. 2013; 87(1): 244-256. doi: 10.1111/1574-6941.12220
18. Telfer A. Singlet Oxygen Production by PSII Under Light Stress: Mechanism, Detection and the Protective role of β-Carotene. Plant and Cell Physiology. 2014; 55(7): 1216-1223. doi: 10.1093/pcp/pcu040
19. Nishiyama Y, Allakhverdiev SI, Yamamoto H, et al. Singlet oxygen inhibits the repair of PSII by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry. 2004, 43: 11321-11330. doi: 10.1021/bi036178q
20. Plaza M, Cifuentes A, Ibanez E. In the search of new functional food ingredients from algae. Trends in Food Science & Technology. 2008; 19(1): 31-39. doi: 10.1016/j.tifs.2007.07.012
21. La Barre S, Potin P, Leblanc C, et al. The Halogenated Metabolism of Brown Algae (Phaeophyta), Its Biological Importance and Its Environmental Significance. Marine Drugs. 2010; 8(4): 988-1010. doi: 10.3390/md8040988
22. Oueslati S, Ksouri R, Falleh H, et al. Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk. Food Chemistry. 2012; 132(2): 943-947. doi: 10.1016/j.foodchem.2011.11.072
23. Okuda T, Ito H. Tannins of Constant Structure in Medicinal and Food Plants—Hydrolyzable Tannins and Polyphenols Related to Tannins. Molecules. 2011; 16(3): 2191-2217. doi: 10.3390/molecules16032191
24. Chaubey MG, Patel SN, Sonani RR, et al. Antioxidant, anti-aging and anti-neurodegenerative biomolecules from Cyanobacteria. In Ecophysiology and biochemistry of Cyanobacteria. Springer Nature; 2022. pp. 327-350.
25. Oliver NJ, Rabinovitch-Deere CA, Carroll AL, et al. Cyanobacterial metabolic engineering for biofuel and chemical production. Current Opinion in Chemical Biology. 2016; 35: 43-50. doi: 10.1016/j.cbpa.2016.08.023
26. Rajneesh, Singh SP, Pathak J, et al. Cyanobacterial factories for the production of green energy and value-added products: An integrated approach for economic viability. Renewable and Sustainable Energy Reviews. 2017; 69: 578-595. doi: 10.1016/j.rser.2016.11.110
27. Park SH, Lee K, Jang JW, et al. Metabolic Engineering of Saccharomyces cerevisiae for Production of Shinorine, a Sunscreen Material, from Xylose. ACS Synthetic Biology. 2018; 8(2): 346-357. doi: 10.1021/acssynbio.8b00388
28. Parmar A, Singh NK, Pandey A, et al. Retracted: Cyanobacteria and microalgae: A positive prospect for biofuels. Bioresource Technology. 2011; 102(22): 10163-10172. doi: 10.1016/j.biortech.2011.08.030
29. Sheng J, Vannela R, Rittmann BE. Disruption of Synechocystis PCC 6803 for lipid extraction. Water Science and Technology. 2012; 65(3): 567-573. doi: 10.2166/wst.2012.879
30. Herbert SK, Samson G, Fork DC, et al. Characterization of damage to Photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity. Proceedings of the National Academy of Sciences. 1992; 89(18): 8716-8720. doi: 10.1073/pnas.89.18.8716
31. Wang Y, Branicky R, Noë A, et al. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. Journal of Cell Biology. 2018; 217(6): 1915-1928. doi: 10.1083/jcb.201708007
32. Singh PR, Gupta A, Singh AP, et al. Effects of ultraviolet radiation on cellular functions of the cyanobacterium Synechocystis sp. PCC 6803 and its recovery under photosynthetically active radiation. Journal of Photochemistry and Photobiology B: Biology. 2024; 252: 112866. doi: 10.1016/j.jphotobiol.2024.112866
33. Zhao W, Ye Z, Zhao J. RbrA, a cyanobacterial rubrerythrin, functions as a FNR‐dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC 7120. Molecular Microbiology. 2007; 66(5): 1219-1230. doi: 10.1111/j.1365-2958.2007.05994.x
34. Priya B, Premanandh J, Dhanalakshmi RT, et al. Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics. 2007; 8(1). doi: 10.1186/1471-2164-8-435
35. Wai HH. Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: Use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo. Nucleic Acids Research. 2000; 28(18): 3524-3534. doi: 10.1093/nar/28.18.3524
36. Zamocky M, Furtmüller PG, Obinger C. Evolution of catalases from bacteria to humans. Antioxidants & Redox Signaling. 2008; 10(9): 1527-1548. doi: 10.1089/ars.2008.2046
37. Wood ZA, Schroder E, Harris JR, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences. 2003; 28(1): 32-40. doi: 10.1016/s0968-0004(02)00003-8
38. Zakar T, Laczko-Dobos H, Toth TN, et al. Carotenoids assist in cyanobacterial photosystem II assembly and function. Frontiers in Plant Science. 2016; 7. doi: 10.3389/fpls.2016.00295
39. Françoise LD, Holger T, Marie-Laurence A, et al. Oxidative stress regulation in lichens and its relevance for survival in coastal habitats. Sea Plants; 2014.
40. Huneck S. The significance of lichens and their metabolites. Naturwissenschaften. 1999; 86(12): 559-570. doi: 10.1007/s001140050676
41. Fernández-Moriano C, Gómez-Serranillos MP, Crespo A. Antioxidant potential of lichen species and their secondary metabolites. A systematic review. Pharmaceutical Biology. 2015; 54(1): 1-17. doi: 10.3109/13880209.2014.1003354
42. Gaikwad SB, Mapari SV, Sutar RR, et al. In vitro and in silico studies of lichen compounds atranorin and salazinic acid as potential antioxidant, antibacterial and anticancer agents. Chemistry & Biodiversity. 2023; 20(12). doi: 10.1002/cbdv.202301229
43. Thadhani VM, Choudhary MI, Ali S, et al. Antioxidant activity of some lichen metabolites. Natural Product Research. 2011; 25(19): 1827-1837. doi: 10.1080/14786419.2010.529546
44. Kwong SP, Wang C. Review: Usnic acid-induced hepatotoxicity and cell death. Environmental Toxicology and Pharmacology. 2020; 80: 103493. doi: 10.1016/j.etap.2020.103493
45. Luzina OA, Salakhutdinov NF. Usnic acid and its derivatives for pharmaceutical use: A patent review (2000–2017). Expert Opinion on Therapeutic Patents. 2018; 28(6): 477-491. doi: 10.1080/13543776.2018.1472239
46. Bruno M, Trucchi B, Burlando B, et al. (+)-Usnic acid enamines with remarkable cicatrizing properties. Bioorganic & Medicinal Chemistry. 2013; 21(7): 1834-1843. doi: 10.1016/j.bmc.2013.01.045
47. Solhaug KA, Gauslaa Y. Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia. 1996; 108(3): 412-418. doi: 10.1007/bf00333715
48. Varol M. Parietin as an efficient and promising anti-angiogenic and apoptotic small-molecule from Xanthoria parietina. Revista Brasileira de Farmacognosia. 2019; 29(6): 728-734. doi: 10.1016/j.bjp.2019.04.012
49. Mugas ML, Calvo G, Marioni J, et al. Photosensitization of a subcutaneous tumour by the natural anthraquinone parietin and blue light. Scientific Reports. 2021; 11(1). doi: 10.1038/s41598-021-03339-z
50. Lohézic-Le Dévéhat F, Legouin B, Couteau C, et al. Lichenic extracts and metabolites as UV filters. Journal of Photochemistry and Photobiology B: Biology. 2013; 120: 17-28. doi: 10.1016/j.jphotobiol.2013.01.009
51. Perera RMTD, Herath KHINM, Sanjeewa KKA, et al. Recent reports on bioactive compounds from marine cyanobacteria in relation to human health applications. Life. 2023; 13(6): 1411. doi: 10.3390/life13061411
52. Singh A, Čížková M, Bišová K, et al. Exploring mycosporine-like amino acids (MAAs) as safe and natural protective agents against UV-induced skin damage. Antioxidants. 2021; 10(5): 683. doi: 10.3390/antiox10050683
53. Morone J, Lopes G, Morais J, et al. Cosmetic application of cyanobacteria extracts with a sustainable vision to skincare: Role in the antioxidant and antiaging process. Marine Drugs. 2022; 20(12): 761. doi: 10.3390/md20120761
54. Pérez-Gálvez A, Viera I, Roca M. Carotenoids and chlorophylls as antioxidants. Antioxidants. 2020; 9(6): 505. doi: 10.3390/antiox9060505
55. Jin J, Li C, He L. Down‐regulatory effect of usnic acid on nuclear factor‐κB‐dependent tumor necrosis factor‐α and inducible nitric oxide synthase expression in lipopolysaccharide‐stimulated macrophages RAW 264.7. Phytotherapy Research. 2008; 22(12): 1605-1609. doi: 10.1002/ptr.2531
56. Odabasoglu F, Cakir A, Suleyman H, et al. Gastroprotective and antioxidant effects of usnic acid on indomethacin-induced gastric ulcer in rats. Journal of Ethnopharmacology. 2006; 103(1): 59-65. doi: 10.1016/j.jep.2005.06.043
57. Amo de Paz G, Raggio J, Gómez-Serranillos MP, et al. HPLC isolation of antioxidant constituents from Xanthoparmelia spp. Journal of Pharmaceutical and Biomedical Analysis. 2010; 53(2): 165-171. doi: 10.1016/j.jpba.2010.04.013
58. Kranner I, Cram WJ, Zorn M, et al. Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences. 2005; 102(8): 3141-3146. doi: 10.1073/pnas.0407716102
59. Kosanić M, Ranković B, Stanojković T, et al. Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. LWT—Food Science and Technology. 2014; 59(1): 518-525. doi: 10.1016/j.lwt.2014.04.047
60. Melo MGD, dos Santos JPA, Serafini MR, et al. Redox properties and cytoprotective actions of atranorin, a lichen secondary metabolite. Toxicology in Vitro. 2011; 25(2): 462-468. doi: 10.1016/j.tiv.2010.11.014
61. Manojlović N, Ranković B, Kosanić M, et al. Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine. 2012; 19(13): 1166-1172. doi: 10.1016/j.phymed.2012.07.012
62. Tatipamula VB, Annam SSP, Nguyen HT, et al. Sekikaic acid modulates pancreatic β-cells in streptozotocin-induced Type 2 diabetic rats by inhibiting digestive enzymes. Natural Product Research. 2020; 35(23): 5420-5424. doi: 10.1080/14786419.2020.1775226
63. Bayir Y, Odabasoglu F, Cakir A, et al. The inhibition of gastric mucosal lesion, oxidative stress and neutrophil-infiltration in rats by the lichen constituent diffractaic acid. Phytomedicine. 2006; 13(8): 584-590. doi: 10.1016/j.phymed.2005.07.002
64. Santos LC, Honda NK, Carlos IZ, et al. Intermediate reactive oxygen and nitrogen from macrophages induced by Brazilian lichens. Fitoterapia. 2004; 75(5): 473-479. doi: 10.1016/j.fitote.2004.04.002
65. Baran R, Ivanova N, Jose N, et al. Functional genomics of novel secondary metabolites from diverse cyanobacteria using untargeted metabolomics. Marine Drugs. 2013; 11(10): 3617-3631. doi: 10.3390/md11103617
66. Liao C, Seebeck FP. Convergent evolution of ergothioneine biosynthesis in cyanobacteria. ChemBioChem. 2017; 18(21): 2115-2118. doi: 10.1002/cbic.201700354
67. Kirilovsky D, Kerfeld CA. The orange carotenoid protein in photoprotection of Photosystem II in cyanobacteria. Biochimica et Biophysica Acta (BBA) - Bioenergetics. 2012; 1817(1): 158-166. doi: 10.1016/j.bbabio.2011.04.013
68. Kirilovsky D, Kerfeld CA. Cyanobacterial photoprotection by the orange carotenoid protein. Nature Plants. 2016; 2(12). doi: 10.1038/nplants.2016.180
69. Peers G, Truong TB, Ostendorf E, et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature. 2009; 462(7272): 518-521. doi: 10.1038/nature08587
70. El Bissati K, Delphin E, Murata N, et al. PSII fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2000; 1457(3): 229-242. doi: 10.1016/S0005-2728(00)00104-3
71. Mudimu O, Koopmann IK, Rybalka N, et al. Screening of microalgae and cyanobacteria strains for α-tocopherol content at different growth phases and the influence of nitrate reduction on α-tocopherol production. Journal of Applied Phycology. 2017; 29(6): 2867-2875. doi: 10.1007/s10811-017-1188-1
72. Colombo ML. An update on vitamin E, tocopherol and tocotrienol—Perspectives. Molecules. 2010; 15(4): 2103-2113. doi: 10.3390/molecules15042103
73. Soule T, Garcia-Pichel F, Stout V. Gene expression patterns associated with the biosynthesis of the sunscreen scytonemin in Nostoc punctiforme ATCC 29133 in Response to UVA Radiation. Journal of Bacteriology. 2009; 191(14): 4639-4646. doi: 10.1128/jb.00134-09
74. Zechmann B, Müller M. Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma. 2010; 246(1-4): 15-24. doi: 10.1007/s00709-010-0111-2
75. Cameron JC, Pakrasi HB. Essential Role of glutathione in acclimation to environmental and redox perturbations in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiology. 2010; 154(4): 1672-1685. doi: 10.1104/pp.110.162990
76. Narainsamy K, Farci S, Braun E, et al. Oxidative‐stress detoxification and signalling in cyanobacteria: the crucial glutathione synthesis pathway supports the production of ergothioneine and ophthalmate. Molecular Microbiology. 2016; 100(1): 15-24. doi: 10.1111/mmi.13296
77. Bellini E, Varotto C, Borsò M, et al. Eukaryotic and prokaryotic phytochelatin synthases differ less in functional terms than previously thought: A comparative analysis of Marchantia polymorpha and Geitlerinema sp. PCC 7407. Plants. 2020; 9(7): 914. doi: 10.3390/plants9070914
78. Balzano S, Sardo A, Blasio M, et al. Microalgal metallothioneins and phytochelatins and their potential use in bioremediation. Frontiers in Microbiology. 2020; 11. doi: 10.3389/fmicb.2020.00517
79. Wolfe‐Simon F, Grzebyk D, Schofield O, et al. The role and evolution of superoxide dismutases in algae1. Journal of Phycology. 2005; 41(3): 453-465. doi: 10.1111/j.1529-8817.2005.00086.x
80. Benov L, Kredich NM, Fridovich I. The mechanism of the auxotrophy for sulfur-containing amino acids imposed upon Escherichia coli by superoxide. Journal of Biological Chemistry. 1996; 271(35): 21037-21040. doi: 10.1074/jbc.271.35.21037
81. Ke WT, Dai GZ, Jiang HB, et al. Essential roles of iron superoxide dismutase in photoautotrophic growth of Synechocystis sp. PCC 6803 and heterogeneous expression of marine Synechococcus sp. CC9311 copper/zinc superoxide dismutase within its sodB knockdown mutant. Microbiology. 2014; 160(1): 228-241. doi: 10.1099/mic.0.073080-0
82. Kim JH, Suh KH. Light-dependent expression of superoxide dismutase from cyanobacterium Synechocystis sp. strain PCC 6803. Archives of Microbiology. 2005; 183(3): 218-223. doi: 10.1007/s00203-005-0766-9
83. Raghavan PS, Rajaram H, Apte SK. Nitrogen status dependent oxidative stress tolerance conferred by overexpression of MnSOD and FeSOD proteins in Anabaena sp. strain PCC7120. Plant Molecular Biology. 2011; 77(4-5): 407-417. doi: 10.1007/s11103-011-9821-x
84. Passardi F, Theiler G, Zamocky M, et al. PeroxiBase: The peroxidase database. Phytochemistry. 2007; 68(12): 1605-1611. doi: 10.1016/j.phytochem.2007.04.005
85. Chelikani P, Fita I, Loewen PC. Diversity of structures and properties among catalases. Cellular and Molecular Life Sciences (CMLS). 2004; 61(2): 192-208. doi: 10.1007/s00018-003-3206-5
86. Carpena X, Soriano M, Klotz MG, et al. Structure of the Clade 1 catalase, CatF of Pseudomonas syringae, at 1.8 Å resolution. Proteins: Structure, Function, and Bioinformatics. 2003; 50(3): 423-436. doi: 10.1002/prot.10284
87. Tichy M, Vermaas W. In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. Journal of Bacteriology. 1999; 181(6): 1875-1882. doi: 10.1128/jb.181.6.1875-1882.1999
88. Antonyuk SV, Melik-Adamyan VR, Popov AN, et al. Three-dimensional structure of the enzyme dimanganese catalase from Thermus Thermophilus at 1 Å resolution. Crystallography Reports. 2000; 45(1): 105-116. doi: 10.1134/1.171145
89. Barynin VV, Whittaker MM, Antonyuk SV, et al. Crystal structure of manganese catalase from Lactobacillus plantarum. Structure. 2001; 9(8): 725-738. doi: 10.1016/S0969-2126(01)00628-1
90. Ballal A, Chakravarty D, Bihani SC, et al. Gazing into the remarkable world of non-heme catalases through the window of the cyanobacterial Mn-catalase ‘KatB.’ Free Radical Biology and Medicine. 2020; 160: 480-487. doi: 10.1016/j.freeradbiomed.2020.08.013
91. Poole LB, Reynolds CM, Wood ZA, et al. AhpF and other NADH: Peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. European Journal of Biochemistry. 2000; 267(20): 6126-6133. doi: 10.1046/j.1432-1327.2000.01704.x
92. Rouhier N, Jacquot JP. The plant multigenic family of thiol peroxidases. Free Radical Biology and Medicine. 2005; 38(11): 1413-1421. doi: 10.1016/j.freeradbiomed.2004.07.037
93. Kang SW, Baines IC, Rhee SG. Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. Journal of Biological Chemistry. 1998; 273(11): 6303-6311. doi: 10.1074/jbc.273.11.6303
94. Seo MS, Kang SW, Kim K, et al. Identification of a New Type of Mammalian Peroxiredoxin That Forms an Intramolecular Disulfide as a Reaction Intermediate. Journal of Biological Chemistry. 2000; 275(27): 20346-20354. doi: 10.1074/jbc.m001943200
95. Mishra Y, Chaurasia N, Rai LC. AhpC (alkyl hydroperoxide reductase) from Anabaena sp. PCC 7120 protects Escherichia coli from multiple abiotic stresses. Biochemical and Biophysical Research Communications. 2009; 381(4): 606-611. doi: 10.1016/j.bbrc.2009.02.100
96. Samuilov V, Bezryadnov D, Gusev M, et al. Hydrogen peroxide inhibits the growth of cyanobacteria. Biochemistry. 1999; 64(1): 47-53.
97. Nair S, Finkel SE. Dps Protects Cells against Multiple Stresses during Stationary Phase. Journal of Bacteriology. 2004; 186(13): 4192-4198. doi: 10.1128/jb.186.13.4192-4198.2004
98. Sato N, Moriyama T, Toyoshima M, et al. The all0458/lti46.2 gene encodes a low temperature-induced Dps protein homologue in the cyanobacteria Anabaena sp. PCC 7120 and Anabaena variabilis M3. Microbiology. 2012; 158(10): 2527-2536. doi: 10.1099/mic.0.060657-0
99. Peña MMO, Bullerjahn GS. The DpsA Protein of Synechococcus sp. Strain PCC7942 Is a DNA-binding Hemoprotein. Journal of Biological Chemistry. 1995; 270(38): 22478-22482. doi: 10.1074/jbc.270.38.22478
100. Banerjee M, Raghavan PS, Ballal A, et al. Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC7120. Photosynthesis Research. 2013; 118(1-2): 59-70. doi: 10.1007/s11120-013-9929-8
101. Penning TM. The aldo-keto reductases (AKRs): Overview. Chemico-Biological Interactions. 2015; 234: 236-246. doi: 10.1016/j.cbi.2014.09.024
102. Jez JM, Penning TM. The aldo-keto reductase (AKR) superfamily: An update. Chemico-Biological Interactions. 2001; 130-132: 499-525. doi: 10.1016/S0009-2797(00)00295-7
103. Sanli G, Dudley JI, Blaber M. Structural biology of the aldo-keto reductase family of enzymes. Cell Biochemistry and Biophysics. 2003; 38: 79-101. doi: 10.1385/CBB:38:1:79
104. Barski OA, Tipparaju SM, Bhatnagar A. The Aldo-Keto Reductase Superfamily and its Role in Drug Metabolism and Detoxification. Drug Metabolism Reviews. 2008; 40(4): 553-624. doi: 10.1080/03602530802431439
105. Marteyn B, Sakr S, Farci S, et al. The Synechocystis PCC6803 MerA-Like Enzyme Operates in the Reduction of Both Mercury and Uranium under the Control of the Glutaredoxin 1 Enzyme. Journal of Bacteriology. 2013; 195(18): 4138-4145. doi: 10.1128/jb.00272-13
106. Zaffagnini M, Bedhomme M, Marchand CH, et al. Redox Regulation in Photosynthetic Organisms: Focus on Glutathionylation. Antioxidants & Redox Signaling. 2012; 16(6): 567-586. doi: 10.1089/ars.2011.4255
107. Rendon JL, Calcagno M, Mendoza-Hernandez G, Ondarza RN. Purification, properties, and oligomeric structure of glutathione reductase from the cyanobacterium Spirulina maxima. Archives of Biochemistry and Biophysics. 1986; 248(1): 215-223. doi:10.1016/0003-9861(86)90419-4
108. Bernroitner M, Zamocky M, Furtmüller PG, et al. Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. Journal of Experimental Botany. 2009; 60(2): 423-440. doi: 10.1093/jxb/ern309
109. Margis R, Dunand C, Teixeira FK, et al. Glutathione peroxidase family—An evolutionary overview. The FEBS Journal. 2008; 275(15): 3959-3970. doi: 10.1111/j.1742-4658.2008.06542.x
110. Gaber A, Tamoi M, Takeda T, et al. NADPH-dependent glutathione peroxidase-like proteins (Gpx-1, Gpx-2) reduce unsaturated fatty acid hydroperoxides in Synechocystis PCC 6803. FEBS Letters. 2001; 499(1-2): 32-36. doi: 10.1016/S0014-5793(01)02517-0
111. ShylajaNaciyar M, Karthick L, Prakasam PA, et al. Diversity of glutathione S-transferases (GSTs) in cyanobacteria with reference to their structures, substrate recognition and catalytic functions. Microorganisms. 2020; 8(5): 712. doi: 10.3390/microorganisms8050712
112. Oakley A. Glutathione transferases: A structural perspective. Drug Metabolism Reviews. 2011; 43(2): 138-151. doi: 10.3109/03602532.2011.558093
113. Kammerscheit X, Chauvat F, Cassier-Chauvat C. First in vivo evidence that glutathione-S-transferase operates in photo-oxidative stress in cyanobacteria. Frontiers in Microbiology. 2019; 10. doi: 10.3389/fmicb.2019.01899
114. Carvalho AN, Marques C, Guedes RC, et al. S‐glutathionylation of Keap1: A new role for glutathione S‐transferase pi in neuronal protection. FEBS Letters. 2016; 590(10): 1455-1466. doi: 10.1002/1873-3468.12177
115. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annual Review of Pharmacology and Toxicology. 2005; 45(1): 51-88. doi: 10.1146/annurev.pharmtox.45.120403.095857
116. Kammerscheit X, Hecker A, Rouhier N, et al. Methylglyoxal detoxification revisited: Role of glutathione transferase in model cyanobacterium Synechocystis sp. strain PCC 6803. ASM Journals. mBio. 2020; 11(4). doi: 10.1128/mbio.00882-20
117. Dixon DP, Lapthorn A, Edwards R. Plant glutathione transferases. Genome Biology. 2002; 3(3). doi: 10.1186/gb-2002-3-3-reviews3004
118. Couturier J, Jacquot JP, Rouhier N. Evolution and diversity of glutaredoxins in photosynthetic organisms. Cellular and Molecular Life Sciences. 2009; 66(15): 2539-2557. doi: 10.1007/s00018-009-0054-y
119. Li M, Yang Q, Zhang L, et al. Identification of novel targets of cyanobacterial glutaredoxin. Archives of Biochemistry and Biophysics. 2007; 458(2): 220-228. doi: 10.1016/j.abb.2006.12.010
120. López-Maury L, Heredia-Martínez LG, Florencio FJ. Characterization of TrxC, an atypical thioredoxin exclusively present in cyanobacteria. Antioxidants. 2018; 7(11): 164. doi: 10.3390/antiox7110164
121. Sánchez-Riego AM, Mata-Cabana A, Galmozzi CV, et al. NADPH-thioredoxin reductase C mediates the response to oxidative stress and thermotolerance in the cyanobacterium Anabaena sp. PCC7120. Frontiers in Microbiology. 2016; 7. doi: 10.3389/fmicb.2016.01283
122. Kumar J, Singh VP, Prasad SM. An investigation on involvement of the ascorbate-glutathione cycle in modulating NaCl toxicity in two cyanobacteria photoacclimatized to different photosynthetic active radiation. Algal Research. 2018; 32: 70-78. doi: 10.1016/j.algal.2017.10.019
123. Kargatov AM, Boshkova EA, Chirgadze YN. Novel approach for structural identification of protein family: Glyoxalase I. Journal of Biomolecular Structure and Dynamics. 2017; 36(10): 2699-2712. doi: 10.1080/07391102.2017.1367330
124. Sousa Silva M, Gomes RA, Ferreira AEN, et al. The glyoxalase pathway: the first hundred years… and beyond. Biochemical Journal. 2013; 453(1): 1-15. doi: 10.1042/bj20121743
125. Subedi KP, Choi D, Kim I, et al. Hsp31 of Escherichia coli K‐12 is glyoxalase III. Molecular Microbiology. 2011; 81(4): 926-936. doi: 10.1111/j.1365-2958.2011.07736.x
126. Rabbani N, Thornalley PJ. Methylglyoxal, glyoxalase 1 and the dicarbonyl proteome. Amino Acids. 2010; 42(4): 1133-1142. doi: 10.1007/s00726-010-0783-0
127. Ghosh A, Islam T. Genome-wide analysis and expression profiling of glyoxalase gene families in soybean (Glycine max) indicate their development and abiotic stress specific response. BMC Plant Biology. 2016; 16(1). doi: 10.1186/s12870-016-0773-9
128. Hasim S, Hussin NA, Alomar F, et al. A Glutathione-independent glyoxalase of the DJ-1 superfamily plays an important role in managing metabolically generated methylglyoxal in Candida albicans. Journal of Biological Chemistry. 2014; 289(3): 1662-1674. doi: 10.1074/jbc.m113.505784
129. Shimakawa G, Suzuki m, Yamamoto E, et al. Scavenging systems for reactive carbonyls in the cyanobacterium Synechocystis sp. PCC 6803. Bioscience, Biotechnology, and Biochemistry. 2013; 77(12): 2441-2448. doi: 10.1271/bbb.130554
130. Shimakawa G, Ifuku K, Suzuki Y, et al. Responses of the chloroplast glyoxalase system to high CO2 concentrations. Bioscience, Biotechnology, and Biochemistry. 2018; 82(12): 2072-2083. doi: 10.1080/09168451.2018.1507724
131. Cassier-Chauvat C, Blanc-Garin V, Chauvat F. Genetic, Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Implications. Genes. 2021; 12(4): 500. doi: 10.3390/genes12040500
132. Rai S, Rai R, Singh PK, et al. Alr2321, a multiple stress inducible glyoxalase I of Anabaena sp. PCC7120 detoxifies methylglyoxal and reactive species oxygen. Aquatic Toxicology. 2019; 214: 105238. doi: 10.1016/j.aquatox.2019.105238
133. Batth R, Jain M, Kumari S, Mustafiz A. Glyoxalase system: A glutathione dependent pathway for abiotic stress tolerance in plants. In: Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham; 2017. pp. 235-263.
134. Dhankher OP. Arsenic metabolism in plants: An inside story. New Phytologist. 2005; 168(3): 503-505. doi: 10.1111/j.1469-8137.2005.01598.x
135. Rai AN, Mishra AK, Tiwari DN. Cyanobacteria: From Basic Science to Applications. Academic Press: Cambridge, MA, USA; 2018.
136. Los DA, Suzuki I, Zinchenko VV, et al. Stress responses in Synechocystis: Regulated genes and regulatory systems. In: The Cyanobacteria: Molecular Biology, Genomics and Evolution. Academic Press: Cambridge, MA, USA; 2008.
137. Apel K, Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology. 2004; 55: 373-399. doi: 10.1146/annurev.arplant.55.031903.141701
138. Babele PK, Singh G, Kumar A, et al. Induction and differential expression of certain novel proteins in Anabaena L31 under UV-B radiation stress. Frontiers in Microbiology. 2015; 6. doi: 10.3389/fmicb.2015.00133
139. Katoh H, Asthana RK, Ohmori M. Gene expression in the cyanobacterium Anabaena sp. PCC7120 under desiccation. Microbial Ecology. 2004; 47(2): 164-174. doi: 10.1007/s00248-003-1043-6
140. Seaver LC, Imlay JA. Are Respiratory Enzymes the Primary Sources of Intracellular Hydrogen Peroxide? Journal of Biological Chemistry. 2004; 279(47): 48742-48750. doi: 10.1074/jbc.m408754200
141. Dietz KJ. Peroxiredoxins in Plants and Cyanobacteria. Antioxidants & Redox Signaling. 2011; 15(4): 1129-1159. doi: 10.1089/ars.2010.3657
142. Dietz KJ. The function of peroxiredoxins in plant organelle redox metabolism. Journal of Experimental Botany. 2006; 57(8): 1697-1709. doi: 10.1093/jxb/erj160
143. Singh SC, Sinha RP, Häder D-P. Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozoologica. 2002; 41: 297-308.
144. Billi D, Potts M. Life and death of dried prokaryotes. Research in Microbiology. 2002; 153(1): 7-12. doi: 10.1016/S0923-2508(01)01279-7
145. Schmitt FJ, Renger G, Friedrich T, et al. Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochimica et Biophysica Acta (BBA) - Bioenergetics. 2014; 1837(6): 835-848. doi: 10.1016/j.bbabio.2014.02.005
146. Contreras L, Moenne A, Gaillard F, et al. Proteomic analysis and identification of copper stress-regulated proteins in the marine alga Scytosiphon gracilis (Phaeophyceae). Aquatic Toxicology. 2010; 96(2): 85-89. doi: 10.1016/j.aquatox.2009.10.007
147. Hosoya-Matsuda N, Motohashi K, Yoshimura H, et al. Anti-oxidative Stress System in Cyanobacteria. Journal of Biological Chemistry. 2005; 280(1): 840-846. doi: 10.1074/jbc.m411493200
148. Gelhaye E, Rouhier N, Navrot N, et al. The plant thioredoxin system. Cellular and Molecular Life Sciences. 2005; 62(1): 24-35. doi: 10.1007/s00018-004-4296-4
149. Lemaire SD, Miginiac-Maslow M. The thioredoxin superfamily in Chlamydomonas reinhardtii. Photosynthentic Research. 2004; 82: 203-220. doi: 10.1007/ s11120-004-1091-x
150. Pérez-Pérez ME, Martín-Figueroa E, Florencio FJ. Photosynthetic regulation of the cyanobacterium Synechocystis sp. PCC 6803 thioredoxin system and functional analysis of TrxB (Trx x) and TrxQ (Trx y) thioredoxins. Molecular Plant. 2009; 2(2): 270-283. doi: 10.1093/mp/ssn070
151. Latifi A, Ruiz M, Zhang CC. Oxidative stress in cyanobacteria. FEMS Microbiology Reviews. 2009; 33(2): 258-278. doi: 10.1111/j.1574-6976.2008.00134.x
152. Cakmak I, Horst WJ. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum. 1991; 83(3): 463-468. doi: 10.1111/j.1399-3054.1991.tb00121.x
153. Heath RL, Packer L. Photoperoxidation in isolated chloroplast: I. Kinetics and stiochiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics. 1968; 125(1): 189-198. doi: 10.1016/0003-9861(68)90654-1
154. Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry. 1971; 44(1): 276-287. doi: 10.1016/0003-2697(71)90370-8
155. Kampfenkel K, Vanmontagu M, Inze D. Extraction and Determination of Ascorbate and Dehydroascorbate from Plant Tissue. Analytical Biochemistry. 1995; 225(1): 165-167. doi: 10.1006/abio.1995.1127
156. Pulz O. Photobioreactors: production systems for phototrophic microorganisms. Applied Microbiology and Biotechnology. 2001; 57(3): 287-293. doi: 10.1007/s002530100702
157. Schwartz SJ, Lorenzo TV. Chlorophyll Stability During Continuous Aseptic Processing and Storage. Journal of Food Science. 1991; 56(4): 1059-1062. doi: 10.1111/j.1365-2621.1991.tb14641.x
158. Dismukes GC, Carrieri D, Bennette N, et al. Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Current Opinion in Biotechnology. 2008; 19(3): 235-240. doi: 10.1016/j.copbio.2008.05.007
159. Saini DK, Chakdar H, Pabbi S, et al. Enhancing production of microalgal biopigments through metabolic and genetic engineering. Critical Reviews in Food Science and Nutrition. 2019; 60(3): 391-405. doi: 10.1080/10408398.2018.1533518
160. Rathod JP, Vira C, Lali AM, et al. Metabolic engineering of Chlamydomonas reinhardtii for enhanced β-carotene and lutein production. Applied Biochemistry and Biotechnology. 2019; 190(4): 1457-1469. doi: 10.1007/s12010-019-03194-9
161. Wang H, Liu Y, Gao X, et al. The recombinant β subunit of C-phycocyanin inhibits cell proliferation and induces apoptosis. Cancer Letters. 2007; 247(1): 150-158. doi: 10.1016/j.canlet.2006.04.002
162. Capone DG, Burns JA, Montoya JP, et al. Nitrogen fixation by Trichodesmium spp.: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochemical Cycles. 2005; 19(2). doi: 10.1029/2004gb002331
163. Bolatk AN K, Akmukhanova NR, Zayadan BK, et al. Toxic Cyanobacteria from Various Natural Sources: Isolation and Characteristics. Biotekhnologiya. 2016; 32(3): 57-66. doi: 10.21519/0234-2758-2016-3-57-66
164. Mille-Claire C, Mille D, De-Roeck-Holtzhauer Y, et al. Orange-red colorant comprising a type 1 R-phycoerythrin, its manufacture and use. French Patent Application FR. 1993; 2(690): 452.
165. Guedes AC, Amaro HM, Malcata FX. Microalgae as Sources of Carotenoids. Marine Drugs. 2011; 9(4): 625-644. doi: 10.3390/md9040625
166. Nowruzi B, Sarvari G, Blanco S. The cosmetic application of cyanobacterial secondary metabolites. Algal Research. 2020; 49: 101959. doi: 10.1016/j.algal.2020.101959
167. Riss J, Décordé K, Sutra T, et al. Phycobiliprotein C-phycocyanin from Spirulina platensis is powerfully responsible for reducing oxidative stress and NADPH oxidase expression induced by an atherogenic diet in hamsters. Journal of Agricultural and Food Chemistry. 2007; 55(19): 7962-7967. doi: 10.1021/jf070529g
168. Gao Q, Garcia-Pichel F. Microbial ultraviolet sunscreens. Nature Reviews Microbiology. 2011; 9(11): 791-802. doi: 10.1038/nrmicro2649
169. Stonik VA, Fedorov SN. Cancer preventive marine natural product. Cellular and Genetic Practices for Translational Medicine; 2011.
170. Haoujar I, Cacciola F, Abrini J, et al. The Contribution of Carotenoids, Phenolic Compounds, and Flavonoids to the Antioxidative Properties of Marine Microalgae Isolated from Mediterranean Morocco. Molecules. 2019; 24(22): 4037. doi: 10.3390/molecules24224037
171. Ravishankar D, Rajora AK, Greco F, et al. Flavonoids as prospective compounds for anti-cancer therapy. The International Journal of Biochemistry & Cell Biology. 2013; 45(12): 2821-2831. doi: 10.1016/j.biocel.2013.10.004
172. Zhang G, Zhang Z, Liu Z. Scytonemin inhibits cell proliferation and arrests cell cycle through downregulating Plk1 activity in multiple myeloma cells. Tumor Biology. 2013; 34(4): 2241-2247. doi: 10.1007/s13277-013-0764-5
173. Kang MR, Jo SA, Lee H, et al. Inhibition of Skin Inflammation by Scytonemin, an Ultraviolet Sunscreen Pigment. Marine Drugs. 2020; 18(6): 300. doi: 10.3390/md18060300
174. Itoh T, Koketsu M, Yokota N, et al. Reduced scytonemin isolated from Nostoc commune suppresses LPS/IFNγ-induced NO production in murine macrophage RAW264 cells by inducing hemeoxygenase-1 expression via the Nrf2/ARE pathway. Food and Chemical Toxicology. 2014; 69: 330-338. doi: 10.1016/j.fct.2014.04.019
175. Jha S, Singh VK, Singh AP, et al. The Radiant World of Cyanobacterial Phycobiliproteins: Examining Their Structure, Functions, and Biomedical Potentials. Targets. 2024; 2(1): 32-51. doi: 10.3390/targets2010002
176. Liu Y, Xu L, Cheng N, et al. Inhibitory effect of phycocyanin from Spirulina platensis on the growth of human leukemia K562 cells. Journal of Applied Phycology. 2000; 12(2): 125-130. doi: 10.1023/A:1008132210772
177. Dasgupta T, Banerjee S, Yadav PK, et al. Chemomodulation of carcinogen metabolising enzymes, antioxidant profiles and skin and forestomach papillomagenesis by Spirulina platensis. Molecular and Cellular Biochemistry. 2001; 226(1-2): 27-38. doi: 10.1023/A:1012769215383
178. Cherng SC, Cheng SN, Tarn A, et al. Anti-inflammatory activity of c-phycocyanin in lipopolysaccharide-stimulated RAW 264.7 macrophages. Life Sciences. 2007; 81(19-20): 1431-1435. doi: 10.1016/j.lfs.2007.09.009
179. Huang Z, Guo BJ, Wong RNS, et al. Characterization and antioxidant activity of selenium-containing phycocyanin isolated from Spirulina platensis. Food Chemistry. 2007; 100(3): 1137-1143. doi: 10.1016/j.foodchem.2005.11.023
180. Kelman D, Ben‐Amotz A, Berman‐Frank I. Carotenoids provide the major antioxidant defence in the globally significant N2‐fixing marine cyanobacterium Trichodesmium. Environmental Microbiology. 2009; 11(7): 1897-1908. doi: 10.1111/j.1462-2920.2009.01913.x
181. Martínez-Francés E, Escudero-Oñate C. Cyanobacteria and Microalgae in the Production of Valuable Bioactive Compounds. Microalgal Biotechnology; 2018.
182. Khan Z, Bhadouria P, Bisen P. Nutritional and therapeutic potential of spirulina. Current Pharmaceutical Biotechnology. 2005; 6(5): 373-379. doi: 10.2174/138920105774370607
183. Gerde JA, Wang T, Yao L, et al. Optimizing protein isolation from defatted and non-defatted Nannochloropsis microalgae biomass. Algal Research. 2013; 2(2): 145-153. doi: 10.1016/j.algal.2013.02.001




.jpg)
.jpg)
