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Synthesis, characterization and investigation of algal oxidative effects of water-soluble copper phthalocyanine containing sulfonate groups

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Abstract

In this study, the chemical and algicidal properties of the newly synthesized compound (2) were evaluated and its algal oxidative effects were determined in Arthrospira platensis and Chlorella vulgaris. First, we have reported on the synthesis and characterization of highly water-soluble copper (II) phthalocyanine (2), containing sodium 2-mercaptoethanesulfonate (2) substituents at the peripheral positions. Some spectroscopic techniques were used to characterize the new synthesized compound (2). In terms of biological properties, C. vulgaris were more tolerance to compound (2) than A. platensis depending to growth parameters. When SOD (Superoxide dismutase) activity significantly increased at 0.25 ppb and 1.5 ppb concentrations in A. platensis cultures, it increased at 6 ppb concentration in C. vulgaris cultures. GR (Glutathione reductase) activity decreased at 1 ppb and 1.5 ppb concentrations while APX (Ascorbate peroxidase) activity did not show a significant change at any concentrations in A. platensis cultures. GR activity showed a significant increase at 6 ppb concentration, while APX activity increased at all concentrations compared to control in C. vulgaris cultures. MDA (malondialdehyde) and H2O2 content decreased at 1 and 1.5 ppb concentrations but there were significant increases in the proline content at all concentrations compared to the control in A. platensis. MDA, H2O2 and free proline contents showed a significant increase at 0.5 ppb concentration in C. vulgaris. In conclusion, compound (2) have algicidal effects, and also it causes to oxidative stress in these organisms.

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References

  1. Segalla A, Borsarelli CD, Braslavsky SE, Spikes JD, Roncucci G, Dei D, Chiti G, Jori G, Reddi E (2002) Photophysical, photochemical and antibacterial photosensitizing properties of a novel octacationic Zn (II)-phthalocyanine. Photochem Photobiol Sci 1:641–648

    Article  PubMed  CAS  Google Scholar 

  2. De La Torre G, Classens CHG, Torres T (2007) Phthalocyanines: old dyes, new materials. Putting color in nanotechnology. Chem Commun 20:2000–2015

    Article  Google Scholar 

  3. Leznoff CC, Lever ABP (1996) Phthalocyanines. Properties and applications. VCH Publishers (LSK) Ltd, Cambridge, pp 1–4

    Google Scholar 

  4. Kandaz M, Yarasir MN, Guney T, Koca A (2009) Both alcohol and halogenated solvents soluble soft-metal sensor functional phthalocyanines: synthesis, electrochemistry, spectroelectrochemistry. J Porphyr Phthalocyanines 13:712–721

    Article  CAS  Google Scholar 

  5. Cheng Y, Samia AC, Li J, Kenney ME, Resnick A, Burda C (2010) Delivery and efficacy of a cancer drug as a function of the bond to the gold nanoparticle surface. Langmuir 26:2248–2255

    Article  PubMed  CAS  Google Scholar 

  6. Margulis GY, Lim B, Hardin BE, UngerEL YJH, Feckl JM, Fattakhova-Rohlfin D, Bein T, Gratzel M, Sellinger A, McGehee MD (2013) Highly soluble energy relay dyes for dye-sensitized solar cells. Phys Chem Chem Phys 15:11306–11312

    Article  PubMed  CAS  Google Scholar 

  7. Sorokin AB (2013) Phthalocyanine metal complexes in catalysis. Chem Rev 113:8152–8191

    Article  PubMed  CAS  Google Scholar 

  8. Venkatramaiah N, Rocha DMGC, Srikanth P, Almeida Paz FA, Tomé JPC (2015) Synthesis and photophysical characterization of dimethylamine-derived Zn (II) phthalocyanines: exploring their potential as selective chemosensors for trinitrophenol. J Mater Chem C 3:1056–1067

    Article  CAS  Google Scholar 

  9. Basova T, Hassan A, Durmus M, Gürek AG, Ahsen V (2016) Liquid crystalline metal phthalocyanines: structural organization on the substrate surface. Coord Chem Rev 310:131–153

    Article  CAS  Google Scholar 

  10. Kalhotka L, Hrdinova Z, Korinkova R, Prichastalova J, Konecna M, Kubac L, Lev J (2012) Test of phthalocyanines antimicrobial activity. Nanocon. http://nanocon2014.tanger.cz/files/proceedings/04/reports/763.pdf. Accessed 9 Dec 2020

  11. Spikes JD (1986) Phthalocyanines as photosensitizers in biological systems and for the photodynamic therapy of tumors. Photochem Photobiol 43(6):691–699

    Article  PubMed  CAS  Google Scholar 

  12. Zhu L, Jing X, Song LB, Liu B, ZhouY XiangY, Xia D (2014) Solid-phase synthesis and catalytic sweetening performance of sulfonated cobalt phthalocyanine from sulfonated phthalic anhydride mixture. New J Chem 38:663–668

    Article  CAS  Google Scholar 

  13. Polony R, Reinert G, Holzle G, Pugin A, Vonderwahl R (1982) Process for combating micro-organisms, and novel phthalocyanine compounds US Patent No. 4,318,883. US Patent and Trademark Office, Washington

  14. Chan WS, Marshall JF, Hart IR (1987) Photodynamic therapy of a murine tumor following sensitization with chloro aluminum sulfonated phthalocyanine. Photochem Photobiol 46:867–871

    Article  PubMed  CAS  Google Scholar 

  15. Sheng C, Pogue BW, Wang E, Hutchins JE, Hoopes PJ (2004) Assessment of photosensitizer dosimetry and tissue damage assay for photodynamic therapy in advanced-stage tumors. Photochem Photobiol 79:520–525

    Article  PubMed  CAS  Google Scholar 

  16. Jori G, Brown SB (2004) Photosensitized inactivation of microorganisms. Photochem Photobiol Sci 3:4003–4005

    Article  Google Scholar 

  17. Calzavara-Pinton PG, Venturini M, Sala R (2005) A comprehensive overview of photodynamic therapy in the treatment of superficial fungal infections of the skin. J Photochem Photobiol B Biol 78:1–6

    Article  CAS  Google Scholar 

  18. Wagner JR, Ali H, Langlois R, Brasseur N, van Lier JE (1987) Biological activities of phthalocyanines-VI. Photooxidation of l-tryptophan by selectively sulfonated gallium phthalocyanines: singlet oxygen yields and effect of aggregation. Photochem Photobiol 45:587–594

    Article  PubMed  CAS  Google Scholar 

  19. Claessens CG, Hahn U, Torres T (2008) Phthalocyanines: from outstanding electronic properties to emerging applications. Chem Rec 8:75–97

    Article  PubMed  CAS  Google Scholar 

  20. Sigler K, Chaloupka J, Brozmanova J, Stadler N, Hofer M (1999) Oxidative stress in microorganisms-I-microbial vs. higher cells—damage and defenses in relation to cell aging and death. Folia Microbiol 44:587–624

    Article  CAS  Google Scholar 

  21. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plan 100:224–233

    Article  CAS  Google Scholar 

  22. Valentine JS, Wertz DL, Lyons TJ, Liou LL, Goto JJ, Gralla EB (1998) The dark side of dioxygen biochemistry. Curr Opin Chem Biol 2:253–262

    Article  PubMed  CAS  Google Scholar 

  23. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Biol 49(1):249–279

    Article  CAS  Google Scholar 

  24. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278(47):46869–46877

    Article  PubMed  CAS  Google Scholar 

  25. Contour-Ansel D, Torres-Franklin ML, Cruz De Carvalho MH, D’Arcy-Lameta A, Zuily-Fodil Y (2006) Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment. Ann Bot 98(6):1279–1287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Anjum NA, Umar S, Chan MT (eds) (2010) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Berlin

    Google Scholar 

  27. Altınışık M (2000) Free oxygen radicals and antioxidants. Tıp Fak, Aydın

    Google Scholar 

  28. Schobert B, Tschesche H (1978) Unusual solution properties of proline and its interaction with proteins. Biochimica et Biophysica Acta (BBA) Gen Subj 541(2):270–277

    Article  CAS  Google Scholar 

  29. Arakawa T, Timasheff S (1983) Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arc Biochem Biophys 224(1):169–177

    Article  CAS  Google Scholar 

  30. Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47(3):411–414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Kandpal RP, Rao NA (1985) Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine coracana) seedlings during water stress and the effect of proline on protein biosynthesis. Plant Sci 40(2):73–79

    Article  CAS  Google Scholar 

  32. Villanueva U, Raposo JC, Castro K, de Diego A, Arana G, Madariaga JM (2008) Raman spectroscopy speciation of natural and anthroplogenic solid phases in river and estuarine sediments with appreciable amount of clay and organic matter. J Raman Spectr 39:1195–1203

    Article  CAS  Google Scholar 

  33. Jančula D, Maršálek B (2012) The toxicity of phthalocyanines to the aquatic plant Lemna minor (duckweed)—testing of 31 compounds. Chemosphere 88(8):962–965

    Article  PubMed  Google Scholar 

  34. Kotronarou A, Hoffmann MR (1991) Catalytic autoxidation of hydrogen-sulfide in waste-water. Environ Sci Technol 25:1153–1160

    Article  CAS  Google Scholar 

  35. Safarik I (1995) Removal of organic polycyclic compounds from water solutions with a magnetic chitosan based sorbent bearing copper phthalocyanine dye. Water Res 29:101–105

    Article  CAS  Google Scholar 

  36. Drabkova M, Marsale B, Admiraal W (2007) Photodynamic therapy against cyanobacteria. Environ Toxicol 22:112–115

    Article  PubMed  CAS  Google Scholar 

  37. Jancula D, Drabkova M, Cerny J, Karaskova M, Korinkov R, Rakusan J, Marsalek B (2008) Algicidal activity of phthalocyanines—screening of 31 compounds. Environ Toxicol 23:218–223

    Article  PubMed  CAS  Google Scholar 

  38. Jančula D, Maršálek B, Novotná Z, Černý J, Karásková RJ (2009) In search of the main properties of phthalocyanines participating in toxicity against cyanobacteria. Chemosphere 77(11):1520–1525

    Article  PubMed  Google Scholar 

  39. Günsel A, Tunca H, Bilgiçli AT, Doğru A, Yaraşir MN, Sevindik TO, Er Ş (2018) The effects of a water-soluble alpha tetra-substituted zinc phthalocyanine derivative on Arthrospira platensis-M2 strain. J Porphyr Phthalocyanines 22(08):686–692

    Article  Google Scholar 

  40. Günsel A, Bilgiçli AT, Barut B, Taslimi P, Özel A, Gülçin İ, Biyiklioglu Z, Yarasir MN (2020) Synthesis of water soluble tetra-substituted phthalocyanines: investigation of DNA cleavage, cytotoxic effects and metabolic enzymes inhibition. J Mol Struct 1214:128210

    Article  Google Scholar 

  41. Aiba S, Ogawa T (1977) Assessment of growth yield of a bluegreen alga, Spirulina platensis, in axenic and continuous culture. Microbiology 102:179–182

    Google Scholar 

  42. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111(1):1–61

    Article  Google Scholar 

  43. MacKinney G (1941) Absorption of light by chlorophyll solution. J Biol Chem 140:315–322

    Article  CAS  Google Scholar 

  44. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  45. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  PubMed  CAS  Google Scholar 

  46. Önem B, Doğru A, Ongun Sevindik T, Tunca H (2018) Preliminary study on the effects of heavy metals on the growth and some antioxidant enzymes in Arthrospira platensis-M2 strain. Phycol Res 66(1):23–30

    Article  Google Scholar 

  47. Wang S, Jiao H, Faust M (1991) Changes in ascorbate, glutathione and related enzyme activity during thidiazuron-induced bud break of apple. Physiol Plant 82:231–236

    Article  CAS  Google Scholar 

  48. Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35:561–565

    Article  CAS  Google Scholar 

  49. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  PubMed  CAS  Google Scholar 

  50. Tunca H, Doğru A, Köçkar F, Önem B, Sevindik TO (2020) Evaluation of Azadirachtin on Arthrospira plantensis Gomont growth parameters and antioxidant enzymes. Int J Limnol 56:8

    Article  Google Scholar 

  51. Weimberg R (1987) Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiol Plant 70(3):381–388

    Article  CAS  Google Scholar 

  52. Ogunsipe A, Nyokong T (2005) Photophysical and photochemical studies of sulphonated non-transition metal phthalocyanines in aqueous and non-aqueous media. J Photochem Photobiol A Chem 173:211–220

    Article  CAS  Google Scholar 

  53. Çamur M, Durmuş M, Bulut M (2011) Synthesis, characterization and comparative studies on the photophysical and photochemical properties of metal-free and zinc(II) phthalocyanines with phenyloxyacetic acid functionalities. Polyhedron 30:1935–1944

    Article  Google Scholar 

  54. Khene S, Ogunsipe A, Antunes E, Nyokong T (2007) Microwave synthesis and photophysics of new tetrasulfonated tin (II) macrocycles. J Porphyr Phthalocyanines 11:109–117

    Article  CAS  Google Scholar 

  55. Mack J, Kobayashi N (2011) Low symmetry phthalocyanines and their analogues. Chem Rev 111:281–321

    Article  PubMed  CAS  Google Scholar 

  56. Bilgiçli AT, Günsel A, Kandaz M, Özkaya AR (2012) Highly selective thioalcohol modified phthalocyanine sensors for Ag(I) and Pd(II) based on target induced J- and H-type aggregations: synthesis, electrochemistry and peripheral metal ion binding studies. Dalton Trans 41:7047

    Article  PubMed  Google Scholar 

  57. Codd GA, Schmid GH, Kowallik W (1972) Enzymic evidence for peroxisomes in a mutant of Chlorella vulgaris. Archiv für Mikrobiol 81(3):264–272

    Article  CAS  Google Scholar 

  58. Miranda MS, Sato S, Mancini-Filho J (2001) Antioxidant activity of the microalga Chlorella vulgaris cultured on special conditions. Boll Chim Farm 140:165–168

    PubMed  CAS  Google Scholar 

  59. Kudaa T, Tsunekawaa M, Gotoa H, Arakib Y (2005) Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. J Food Comp Anal 18:625–633

    Article  Google Scholar 

  60. Wu LC, Ho JAA, Shieh MC, Lu IW (2005) Antioxidant and antiproliferative activities of Spirulina and Chlorella water extracts. J Agric Food Chem 53:4207–4212

    Article  PubMed  CAS  Google Scholar 

  61. Vijayavel K, Anbuselvam C, Balasubramanian MP (2007) Antioxidant effect of the marine algae Chlorella vulgaris against naphthalene-induced oxidative stress in the albino rats. Mol Cel Biochem 303(1–2):39–44

    Article  CAS  Google Scholar 

  62. Sabatini SE, Juárez AB, Eppis MR, Bianchi L, Luquet CM, de Molina RMDC (2009) Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206

    Article  PubMed  CAS  Google Scholar 

  63. Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160(2):291–299

    Article  PubMed  CAS  Google Scholar 

  64. Stauber JL, Florence TM (1987) Mechanism of toxicity of ionic copper and copper complexes to algae. Mar Biol 94(4):511–519

    Article  CAS  Google Scholar 

  65. Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Pawlik-Skowrońska B (2003) When adapted to high zinc concentrations the periphytic green alga Stichococcus tenue produces high amounts of novel phytochelatin-related peptides. Aquat Toxicol 62:155–163

    Article  PubMed  Google Scholar 

  67. Ashraf MFMR, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216

    Article  CAS  Google Scholar 

  68. Banu MNA, Hoque MA, Watanabe-Sugimoto M, Islam MM, Uraji M, Matsuoka K, Murata Y (2010) Proline and glycinebetaine ameliorated NaCl stress via scavenging of hydrogen peroxide and methylglyoxal but not superoxide or nitric oxide in tobacco cultured cells. Biosci Biotechnol Biochem 74(10):2043–2049

    Article  PubMed  CAS  Google Scholar 

  69. Kavitha K, Venkataraman G, Parida A (2008) An oxidative and salinity stress induced peroximal ascorbate peroxidase from Avicennia marina: molecular and functional characterization. Plant Physiol Biochem 46:794–804

    Article  PubMed  CAS  Google Scholar 

  70. Okamoto OK, Pinto E, Latorre LR, Bechara EJH, Colepicolo P (2001) Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Contam Toxicol 40:18–24

    Article  PubMed  CAS  Google Scholar 

  71. Suman TY, Rajasree SRR, Kirubagaran R (2015) Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol Environ Saf 113:23–30

    Article  PubMed  CAS  Google Scholar 

  72. Hamed SM, Selim S, Klöck G, AbdElgawad H (2017) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotoxicol Environ Saf 144:19–25

    Article  PubMed  CAS  Google Scholar 

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Funding

This study was supported by Sakarya University Research Projects under Grant no. FBETEZ- 2018-2-7-172 and HIZDEP- 2019-5-19-77.

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Tekbaba, A., Özpınar, S.Ç., Tunca, H. et al. Synthesis, characterization and investigation of algal oxidative effects of water-soluble copper phthalocyanine containing sulfonate groups. J Biol Inorg Chem 26, 355–365 (2021). https://doi.org/10.1007/s00775-021-01860-0

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