Evaluation of Oxidative Stress And Growth Alterations on Arthrospira Platensis Gomont and Chlorella Vulgaris Beijerinck (Beijerinck) by Cambio
Yıl 2023,
, 1120 - 1134, 31.10.2023
Şükrüye Er
,
Hatice Tunca
,
Ali Doğru
,
Tuğba Ongun Sevindik
Öz
This study aims to evaluate the toxicity effects of different concentrations of Cambio on Chlorella vulgaris (0-500 μg mL-1) and Arthrospira platensis (0-50 μg mL-1) algae by determining the changes in chlorophyll-a amount, OD 750 (biomass) and antioxidant parameters (the activities of Superoxide dismutase (SOD), Ascorbate peroxidase (APX), Glutathione reductase (GR) and the contents of malondialdehyde (MDA), hydrogen peroxide (H2O2), proline). A. platensis is being a cyanobacterium used commercially because of its high nutrient content. C. vulgaris used for medical and commercial purposes due to the capability of bioremediation, the structure of drug raw material, and nutrient compound. Ecotoxicological studies on these cosmopolitan algae are important for determining the harmful effects of chemicals on freshwater ecosystems. Cambio was toxic to A. platensis cells at the highest concentration, however, it stimulated the growth of C. vulgaris. For A. platensis application, the activity of Superoxide dismutase significantly decreased at moderate concentrations (p<0.05), while the activity of Ascorbate peroxidase decreased at the highest concentration (p<0.05). Moreover, the activity of Glutathione reductase rose at 20 μg mL-1 concentration. Malondialdehyde and H2O2 did not show significant changes, but the proline content showed significant increases in all Cambio concentrations compared to the control (p<0.05). However, for C. vulgaris application the antioxidant parameters did not show any alterations. These results are indicated that the effects of Cambio on A. platensis are more destructive than C. vulgaris.
Destekleyen Kurum
Sakarya Üniversitesi, BAP
Proje Numarası
2018-02- 09-173
Teşekkür
The authors would like to thank to Prof. Dr. Oya Işık from Çukurova University,
Faculty of Fisheries for providing us C. vulgaris culture, and also, to Sakarya University
Research Foundation for financially supporting this research
Kaynakça
- Aiba, S. & Ogawa, T. (1977). Assessment of growth yield of a blue-green alga, Spirulina platensis, in axenic and continuous culture. Journal of General Microbiology, 102, 179-182.
- Anjum, N.A., Umar, S. & Chan, M.T. (2010). Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer science- Bussiness Media. 91-113.
- Aysel, V. (2005). Checklist of the Freshwater Algae of Turkey. Journal of the Black Sea/Mediterranean Environment, 11, 1-124.
- Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environmental Experimental Botany, 68 (2), 175-179.
- Beyer, W. F. & Fridovich, I. (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry, 161, 559–566.
- Bhatnagar- Mathur, P., Vadez, V. & Sharma, K.K. (2008). Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Reports, 27, 411–424.
- Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72, 248-254.
- Bozic, D., Vrbnicanin, S., Stojicevic, D. & Pavlovic, D. (2016). Effect of nicosulfuron on the populations of invasive weedy sunflower. 27. Deutsche Arbeitsbesprechung über Fragen der Unkrautbiologie und -bek.mpfung, 23.-25. February 2016 Braunschweig, Germany.
- Cao, Q., Sun, W., Yang, T., Zhu, Z., Jiang, Y., Hu, W., ... & Yang, H. (2022). The toxic effects of polystyrene microplastics on freshwater algae Chlorella pyrenoidosa depends on the different size of polystyrene microplastics. Chemosphere, 308, 136135.
- Cedergreen, N. & Streibig, J.C. (2005). The toxicity of herbicides to non‐target aquatic plants and algae: assessment of predictive factors and hazard. Pest Management Science 61(12). 1152-1160.
- Choudhary, M., Jetley, U.K., Khan, M.A., Zutshi, S. & Fatma, T. (2007). Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicology and Environmental Safety, 66, 204–209.
- Delorenzo, M.E., Scott, G.I., & Ross, P.E. (2001). Toxicity of pesticides to aquatic microorganisms: A Review Environmental Toxicology and Chemistry, 20(1), 84–98.
- EPA. (2004) – US Environmental Protection Agency. Report of the Food Quality Protection Act (FQPA) Tolerance Reassessment Progress and Risk Management Decision (TRED) for Nicosulfuron.
- Freire, V. A. F., de Melo, A. D., de Lima Santos, H., & de Barros Pinheiro, M. (2023). Evaluation of oxidative stress markers in subtypes of preeclampsia: A systematic review and meta-analysis. Placenta, 132, 55-62.
- Geoffroy, L., Teisseire, H., Couderchet, M. & Vernet. G. (2002). Effect of oxyfluorfen and diuron alone and in mixture on antioxidative enzymes of Scenedesmus obliquus. Pesticide Biochemistry and Physiology, 72, 178–185.
- Gökpınar, S., Koray, T., Akcicek, E., Göksan, T. & Durmaz, Y. (2006). Algal antioksidanlar. Ege Üniversitesi Su Ürünleri Dergisi, 23, 85-89.
- Hasannuzzaman, M., Hossain, M.A., Da Silva, J.A.T. & Fujita, M. (2012). Plant Response and Tolerance to Abiotic Oxidative Stress: Antioxidant Defense Is a Key Factor. Crop Stress and its Management: Perspectives ans Strategies. Springer.
- Heath, R.L. & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 1086 (125),189-198.
- Ighodaro, O.A. & Akinloye, O.A. (2017). First-line defense antioxidants-superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defense grid.
Alexandria Journal of Medicine, 54 (4), 287-293
- Kookal, S. K., Nawkarkar, P., Gaur, N. A., & Kumar, S. (2023). Bioremediation of ethanol wash by microalgae and generation of bioenergy feedstock. Journal of Applied Phycology, 35(1), 183-194.
- Kumar, S., Jetley, U.K. & Fatma, T. (2004). Tolerance of Spirulina platensis- S5 and Anabaena sp., to endosulfan an organochlorine pesticide. Annual Plant Physiology, 18(2), 103-107.
- Kumar, S., Habib, K. & Fatma, T. (2008). Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria. Science of The Total Environment, 403 (1–3), 130-138.
- Lynch, M., & Marinov, G. (2018). Correction: membranes, energetics, and evolution across the prokaryote-eukaryote divide. Evolutionary Biology,1-30.
- Ma, J., Xu, L., Wang, S., Zheng, R., Jin, S., Huang, S. & Huang, Y. (2002). Toxicity of 40 herbicides to the green alga Chlorella vulgaris. Ecotoxicology and Environmental Safety, 51, 128-132.
- Mackinney, Q. (1941). Absorption of light by chlorophyll solutions. Journal of Biological Chemistry, 140, 315-322.
- Mittler, R., Zandalinas, S. I., Fichman, Y., & Van Breusegem, F. (2022). Reactive oxygen species signalling in plant stress responses. Nature Reviews Molecular Cell Biology, 23(10), 663-679.
- Mallick, N. & Mohn, F. H. (2000). Reactive oxygen species: response of algal cells. Journal of Plant Physiology, 157, 183-193.
- Niedobová, J., Ouředníčková, J., Michalko, R., & Skalský, M. (2022). The toxicity of the glyphosate herbicide for Pardosa spiders’ predatory activity depends on the formulation of the glyphosate product. Environmental Chemistry Letters, 20(2), 983-990.
- Neilson, A. H. & Larson, T. (1980). The utilization of organic nitrogen for growth of algae: physiological aspects. Physiology Plantarum, 48, 542–553.
- Nyström, B., Björbsäter, B. & Blanck, H. (1999). Effects of sulfonylurea herbicides on non-target aquatic micro-organisms. Growth inhibition of micro-algae and short-term inhibition of adenine and thymidine
incorporation in periphyton communities. Aquatic Toxicology, 47, 9–22.
- Özyurt, M., Kopar, H., Özyurt, S., Demirhan, İ. & Belge Kurutaş, E. (2021). Menengiç, Işgın ve Çiriş Otu’nda Antioksidan Aktivitenin Araştırılması. KSÜ Tarım ve Doğa Derg 24 (4), 733-737.
- Phetchuay, P., Peerakietkhajorn, S., Duangpan, S., & Buapet, P. (2019). Toxicity effects of copper and zinc on the photosynthetic efficiency and oxidative stress-related parameters of the green alga Chlorella vulgaris Beijerinck. Journal of Fisheries and Environment, 43(2), 14-26.
- PMRA-ARLA. (1996). Decision document: nicosulfuron. Canada: Pesticide Management and Regulation Agency. (42 pp.) http://www.hc-sc.gc.ca/ pmra-arla/e9601e.pdf. (Accessed: 23.20.2021)
- Relyea, R. A. (2005). The Impact of Insecticides and Herbicides on the Biodiversity and Productivity of Aquatic Communities. Ecological Applications, 15 (2), 618-627.
- Rezayian, M., Niknam, V., & Ebrahimzadeh, H. (2019). Oxidative damage and antioxidative system in algae. Toxicology reports, 6, 1309-1313.
- Rey-Caballero, J., Menéndez, J., Giné-Bordonaba, J., Salas, M., Alcántara, R., & Torra, J. (2016). Unravelling the resistance mechanisms to 2, 4-D (2, 4-dichlorophenoxyacetic acid) in corn poppy (Papaver rhoeas). Pesticide Biochemistry and Physiology, 133, 67-72.
- Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology, 111, 1-61.
- Qian, H., Chen, W., Sheng, G. D., Xu, X., Liu, W. & Fu, Z. (2008). Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquatic
Toxicology, 88(4), 301-307.
- Saradhi, A. & Saradhi, P. P. (1991). Proline accumulation under heavy metal stress. Journal of Plant Physiology, 138, 554-558.
- Schmitt-Jansen, M. & Altenburger, R. (2005). Toxic effects of isoproturon on periphyton communities – a microcosm study. Estuarine, Coastal and Shelf Science, 62, 539–545.
- Schuler, L. J. & Gary, M. (2008). Aquatic Risk Assessment of Herbicides in Freshwater Ecosystems of South Florida. Archives of Environmental Contamination Toxicology 54, 571–583.
- Seguin, F., Leboulanger, C., Rimet, F., Druart, J. C. & Bérard, A. (2001). Effects of atrazine and nicosulfuron on phytoplankton in systems of increasing complexity. Archives Environmental Contamination Toxicology 40, 198–208.
- Serim, A. T., Koca, E., Güzel, N. P. & Asav, Ü. (2017). Vejetatif filtre şeritlerinde kullanılabilecek bazı dar yapraklı bitkilerin Rimnosulfuron ve Nicosulfuron’ a toleransı. Turkish Journal of Weed Science, 20 (1), 1-9.
- Sgherri. C. L. M., Loggini, B., Puliga, S. & Navari-Izzo, F. (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration.’ Phytochemistry, 35, 561–565.
- Sili, C., Torzillo, G., & Vonshak, A. (2012). Arthrospira (Spirulina). In Ecology of Cyanobacteria II (pp. 677-705) Dordrecht, Springer.
- Soares, C., Fernandes, B., Paiva, C., Nogueira, V., Cachada, A., Fidalgo, F., & Pereira, R. (2023). Ecotoxicological relevance of glyphosate and flazasulfuron to soil habitat and retention functions–Single vs combined exposures. Journal of Hazardous Materials, 442, 130128.
- Sultan, S. & Fatma, T. (1999). Phytotoxicity of heavy metals on Spirulina platensis. Phykos, 38(1-2), 87- 92.
- Tang, J., Liang, Q., Li, C., Huang, X., Xian, X., Li, J., ... & Zhang, R. (2022). Application of Marine Algae in Water Pollution Control. In IOP Conference Series: Earth and Environmental Science (Vol. 966, No. 1, p. 012001). IOP Publishing.
- Tamil Selvan, S., Dakshinamoorthi, B. M., Chandrasekaran, R., Muthusamy, S., Ramamurthy, D., & Balasundaram, S. (2023). Integrating eco-technological approach for textile dye effluent treatment and carbon dioxide capturing from unicellular microalga Chlorella vulgaris RDS03: a synergistic method. International Journal of Phytoremediation, 25(4), 466-482.
- Tunca, H., Doğru, A., Köçkar, F., Önem, B. & Sevindik, T. O. (2020). Evaluation of Azadirachtin on Arthrospira plantensis Gomont growth parameters and antioxidant enzymes. Annales de Limnologie-International Journal of Limnology, 56, 1-8.
- Tunca, H., Özpınar, S. Ç., Tekbaba, A. G., Sevindik, T. O., Günsel, A., Bilgiçli, A. T., & Yaraşır, M. N. (2022). Algaecidal and oxidative effects of metal-free phthalocyanine beta tetra-substituted with sodium 2-mercaptoethanesulfonate. Turkish Journal of Chemistry, 46 (2), 367-377.
- Valentine, J. S., Wertz, D. L., Ltons, T. J., Liou, L. L., Goto, J. J. & Gralla, E. B. (1998). The dark side of dioxygen biochemistry. Current Opinion In Chemical Biology, 2, 253-262.
- Vervliet-Scheebaum, M., Alain Straus, A., Horst Tremp, H., Hamer, M., Maund, S. J., Edgar Wagner E & Schulz R (2010). A microcosm system to evaluate the toxicity of the triazine herbicide simazine on aquatic macrophytes. Environmental Pollution 158, 615–623.
- Walsh, G. E. (1978). Toxic Effects of Pollutants on Plankton. Principles of Ecotoxicology. 257-274, USA.
- Wang, H., & Ki, J. S. (2020). Molecular identification, differential expression and protective roles of iron/manganese superoxide dismutases in the green algae Closterium ehrenbergii against metal stress. European Journal of Protistology, 74, 125689.
- Wang, L., Riaz, M., Song, B., Song, X., Huang, W., Bai, X., & Zhao, X. (2022). Study on phytotoxicity evaluation and physiological properties of nicosulfuron on sugar beet (Beta vulgaris L.). Frontiers in Plant Science, 13, 998867.
- Wang, S. Y., Jiao, H., Faust, M. (1991). Changes in ascorbate, glutathione, and related enzyme activity during thidiazuron-induced bud break of apple. Plant Physiology 82: 231-236.
- Wang, Z. H., Xie, J., Jiang, S., Shi, J., Liu, Y. & Gong, W. (2012). Effects of commercial cypermethrin on the growth of Scenedesmus obliquus and its physiochemical responses. China Environmental Science 32 (4): 659-665.
- Weimberg, R. (1987). Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiologia Plantarum 70: 381-388.
- Wu, S., Zhang, H. & Qiu, L. (2014). Toxicological Responses of Chlorella vulgaris to Dichloromethane and Dichloroethane. Environmental Engineering Science 31: 1.
- Wu, Z. X., Xu, N. W., Yang, M., Li, X. L., Han, J. L., Lin, X. H., ... & Wang, J. (2022). Responses of photosynthesis, antioxidant enzymes, and related gene expression to nicosulfuron stress in sweet maize (Zea mays L.). Environmental Science and Pollution Research, 29(25), 37248-37265.
- Xu, L., Zhao, Z., Yan, Z., Zhou, G., Zhang, W., Wang, Y., & Li, X. (2022). Defense pathways of Chlamydomonas reinhardtii under silver nanoparticle stress: Extracellular biosorption, internalization and antioxidant genes. Chemosphere, 291, 132764.
- Yang, Y., Fan, X., Zhang, J., Qiao, S., Wang, X., Zhang, X., ... & Hou, J. (2022). A critical review on the interaction of iron-based nanoparticles with blue-green algae and their metabolites: From mechanisms to applications. Algal Research, 64, 102670.
Cambio'nun Arthrospira Platensis Gomont ve Chlorella Vulgaris Beijerinck (Beijerinck) Üzerinde Oluşturduğu Oksidatif Stresin Ve Büyüme Değişimlerinin Değerlendirilmesi
Yıl 2023,
, 1120 - 1134, 31.10.2023
Şükrüye Er
,
Hatice Tunca
,
Ali Doğru
,
Tuğba Ongun Sevindik
Öz
Bu çalışma, Cambio'nun farklı konsantrasyonlarının Chlorella vulgaris (0-500 μg mL-1) ve Arthrospira platensis (0-50 μg mL-1) alglerinde oluşturduğu biyokütle (klorofil-a miktarı, OD 750) ve antioksidan parametrelerindeki (Süperoksit dismutaz (SOD), Askorbat peroksidaz (APX), glutatyon peroksidaz (GR) enzim aktiviteleri ve malondialdehit (MDA), hidrojen peroksit (H202) ve prolin içerikleri) değişimleri belirlemeyi amaçlamaktadır. A. platensis, yüksek besin içeriği nedeniyle ticari olarak kullanılan bir siyanobakteridir. C. vulgaris, biyoremediasyon kabiliyeti, ilaç hammaddesinin yapısı ve besin bileşimi nedeniyle tıbbi ve ticari amaçlar için kullanılmaktadır. Cambio, en yüksek konsantrasyonda A. platensis hücreleri için toksiktir, ancak C. vulgaris' in büyümesini uyarmıştır. Kozmopolit olan bu iki algin üzerinde yapılan ekotoksikolojik çalışmalar kimyasalların tatlı su ekosistemlerinde meydana getirdiği zararlı etkilerin belirlenmesi adına önemlidir. A. platensis uygulamasında, süperoksit dismutaz aktivitesi orta konsantrasyonlarda; Askorbat peroksidaz aktivitesi ise en yüksek konsantrasyonda anlamlı olarak azalmıştır (p<0.05). Ayrıca, Glutatyon redüktazın aktivitesi, 20 µg mL-1 konsantrasyonunda artış göstermiştir. Malondialdehit ve H2O2 miktarında önemli değişiklikler görülmemiştir. Ancak prolin içeriği, kontrole kıyasla tüm Cambio konsantrasyonlarında önemli artışlar göstermiştir (p<0.05). Ancak C. vulgaris uygulaması için antioksidan parametrelerde herhangi bir değişiklik gözlenmemiştir. Bu sonuçlar Cambio'nun A. platensis üzerindeki etkilerinin C. vulgaris üzerindeki etkilerine göre daha yıkıcı olduğunu göstermektedir.
Proje Numarası
2018-02- 09-173
Kaynakça
- Aiba, S. & Ogawa, T. (1977). Assessment of growth yield of a blue-green alga, Spirulina platensis, in axenic and continuous culture. Journal of General Microbiology, 102, 179-182.
- Anjum, N.A., Umar, S. & Chan, M.T. (2010). Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer science- Bussiness Media. 91-113.
- Aysel, V. (2005). Checklist of the Freshwater Algae of Turkey. Journal of the Black Sea/Mediterranean Environment, 11, 1-124.
- Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environmental Experimental Botany, 68 (2), 175-179.
- Beyer, W. F. & Fridovich, I. (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry, 161, 559–566.
- Bhatnagar- Mathur, P., Vadez, V. & Sharma, K.K. (2008). Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Reports, 27, 411–424.
- Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72, 248-254.
- Bozic, D., Vrbnicanin, S., Stojicevic, D. & Pavlovic, D. (2016). Effect of nicosulfuron on the populations of invasive weedy sunflower. 27. Deutsche Arbeitsbesprechung über Fragen der Unkrautbiologie und -bek.mpfung, 23.-25. February 2016 Braunschweig, Germany.
- Cao, Q., Sun, W., Yang, T., Zhu, Z., Jiang, Y., Hu, W., ... & Yang, H. (2022). The toxic effects of polystyrene microplastics on freshwater algae Chlorella pyrenoidosa depends on the different size of polystyrene microplastics. Chemosphere, 308, 136135.
- Cedergreen, N. & Streibig, J.C. (2005). The toxicity of herbicides to non‐target aquatic plants and algae: assessment of predictive factors and hazard. Pest Management Science 61(12). 1152-1160.
- Choudhary, M., Jetley, U.K., Khan, M.A., Zutshi, S. & Fatma, T. (2007). Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicology and Environmental Safety, 66, 204–209.
- Delorenzo, M.E., Scott, G.I., & Ross, P.E. (2001). Toxicity of pesticides to aquatic microorganisms: A Review Environmental Toxicology and Chemistry, 20(1), 84–98.
- EPA. (2004) – US Environmental Protection Agency. Report of the Food Quality Protection Act (FQPA) Tolerance Reassessment Progress and Risk Management Decision (TRED) for Nicosulfuron.
- Freire, V. A. F., de Melo, A. D., de Lima Santos, H., & de Barros Pinheiro, M. (2023). Evaluation of oxidative stress markers in subtypes of preeclampsia: A systematic review and meta-analysis. Placenta, 132, 55-62.
- Geoffroy, L., Teisseire, H., Couderchet, M. & Vernet. G. (2002). Effect of oxyfluorfen and diuron alone and in mixture on antioxidative enzymes of Scenedesmus obliquus. Pesticide Biochemistry and Physiology, 72, 178–185.
- Gökpınar, S., Koray, T., Akcicek, E., Göksan, T. & Durmaz, Y. (2006). Algal antioksidanlar. Ege Üniversitesi Su Ürünleri Dergisi, 23, 85-89.
- Hasannuzzaman, M., Hossain, M.A., Da Silva, J.A.T. & Fujita, M. (2012). Plant Response and Tolerance to Abiotic Oxidative Stress: Antioxidant Defense Is a Key Factor. Crop Stress and its Management: Perspectives ans Strategies. Springer.
- Heath, R.L. & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 1086 (125),189-198.
- Ighodaro, O.A. & Akinloye, O.A. (2017). First-line defense antioxidants-superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defense grid.
Alexandria Journal of Medicine, 54 (4), 287-293
- Kookal, S. K., Nawkarkar, P., Gaur, N. A., & Kumar, S. (2023). Bioremediation of ethanol wash by microalgae and generation of bioenergy feedstock. Journal of Applied Phycology, 35(1), 183-194.
- Kumar, S., Jetley, U.K. & Fatma, T. (2004). Tolerance of Spirulina platensis- S5 and Anabaena sp., to endosulfan an organochlorine pesticide. Annual Plant Physiology, 18(2), 103-107.
- Kumar, S., Habib, K. & Fatma, T. (2008). Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria. Science of The Total Environment, 403 (1–3), 130-138.
- Lynch, M., & Marinov, G. (2018). Correction: membranes, energetics, and evolution across the prokaryote-eukaryote divide. Evolutionary Biology,1-30.
- Ma, J., Xu, L., Wang, S., Zheng, R., Jin, S., Huang, S. & Huang, Y. (2002). Toxicity of 40 herbicides to the green alga Chlorella vulgaris. Ecotoxicology and Environmental Safety, 51, 128-132.
- Mackinney, Q. (1941). Absorption of light by chlorophyll solutions. Journal of Biological Chemistry, 140, 315-322.
- Mittler, R., Zandalinas, S. I., Fichman, Y., & Van Breusegem, F. (2022). Reactive oxygen species signalling in plant stress responses. Nature Reviews Molecular Cell Biology, 23(10), 663-679.
- Mallick, N. & Mohn, F. H. (2000). Reactive oxygen species: response of algal cells. Journal of Plant Physiology, 157, 183-193.
- Niedobová, J., Ouředníčková, J., Michalko, R., & Skalský, M. (2022). The toxicity of the glyphosate herbicide for Pardosa spiders’ predatory activity depends on the formulation of the glyphosate product. Environmental Chemistry Letters, 20(2), 983-990.
- Neilson, A. H. & Larson, T. (1980). The utilization of organic nitrogen for growth of algae: physiological aspects. Physiology Plantarum, 48, 542–553.
- Nyström, B., Björbsäter, B. & Blanck, H. (1999). Effects of sulfonylurea herbicides on non-target aquatic micro-organisms. Growth inhibition of micro-algae and short-term inhibition of adenine and thymidine
incorporation in periphyton communities. Aquatic Toxicology, 47, 9–22.
- Özyurt, M., Kopar, H., Özyurt, S., Demirhan, İ. & Belge Kurutaş, E. (2021). Menengiç, Işgın ve Çiriş Otu’nda Antioksidan Aktivitenin Araştırılması. KSÜ Tarım ve Doğa Derg 24 (4), 733-737.
- Phetchuay, P., Peerakietkhajorn, S., Duangpan, S., & Buapet, P. (2019). Toxicity effects of copper and zinc on the photosynthetic efficiency and oxidative stress-related parameters of the green alga Chlorella vulgaris Beijerinck. Journal of Fisheries and Environment, 43(2), 14-26.
- PMRA-ARLA. (1996). Decision document: nicosulfuron. Canada: Pesticide Management and Regulation Agency. (42 pp.) http://www.hc-sc.gc.ca/ pmra-arla/e9601e.pdf. (Accessed: 23.20.2021)
- Relyea, R. A. (2005). The Impact of Insecticides and Herbicides on the Biodiversity and Productivity of Aquatic Communities. Ecological Applications, 15 (2), 618-627.
- Rezayian, M., Niknam, V., & Ebrahimzadeh, H. (2019). Oxidative damage and antioxidative system in algae. Toxicology reports, 6, 1309-1313.
- Rey-Caballero, J., Menéndez, J., Giné-Bordonaba, J., Salas, M., Alcántara, R., & Torra, J. (2016). Unravelling the resistance mechanisms to 2, 4-D (2, 4-dichlorophenoxyacetic acid) in corn poppy (Papaver rhoeas). Pesticide Biochemistry and Physiology, 133, 67-72.
- Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology, 111, 1-61.
- Qian, H., Chen, W., Sheng, G. D., Xu, X., Liu, W. & Fu, Z. (2008). Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquatic
Toxicology, 88(4), 301-307.
- Saradhi, A. & Saradhi, P. P. (1991). Proline accumulation under heavy metal stress. Journal of Plant Physiology, 138, 554-558.
- Schmitt-Jansen, M. & Altenburger, R. (2005). Toxic effects of isoproturon on periphyton communities – a microcosm study. Estuarine, Coastal and Shelf Science, 62, 539–545.
- Schuler, L. J. & Gary, M. (2008). Aquatic Risk Assessment of Herbicides in Freshwater Ecosystems of South Florida. Archives of Environmental Contamination Toxicology 54, 571–583.
- Seguin, F., Leboulanger, C., Rimet, F., Druart, J. C. & Bérard, A. (2001). Effects of atrazine and nicosulfuron on phytoplankton in systems of increasing complexity. Archives Environmental Contamination Toxicology 40, 198–208.
- Serim, A. T., Koca, E., Güzel, N. P. & Asav, Ü. (2017). Vejetatif filtre şeritlerinde kullanılabilecek bazı dar yapraklı bitkilerin Rimnosulfuron ve Nicosulfuron’ a toleransı. Turkish Journal of Weed Science, 20 (1), 1-9.
- Sgherri. C. L. M., Loggini, B., Puliga, S. & Navari-Izzo, F. (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration.’ Phytochemistry, 35, 561–565.
- Sili, C., Torzillo, G., & Vonshak, A. (2012). Arthrospira (Spirulina). In Ecology of Cyanobacteria II (pp. 677-705) Dordrecht, Springer.
- Soares, C., Fernandes, B., Paiva, C., Nogueira, V., Cachada, A., Fidalgo, F., & Pereira, R. (2023). Ecotoxicological relevance of glyphosate and flazasulfuron to soil habitat and retention functions–Single vs combined exposures. Journal of Hazardous Materials, 442, 130128.
- Sultan, S. & Fatma, T. (1999). Phytotoxicity of heavy metals on Spirulina platensis. Phykos, 38(1-2), 87- 92.
- Tang, J., Liang, Q., Li, C., Huang, X., Xian, X., Li, J., ... & Zhang, R. (2022). Application of Marine Algae in Water Pollution Control. In IOP Conference Series: Earth and Environmental Science (Vol. 966, No. 1, p. 012001). IOP Publishing.
- Tamil Selvan, S., Dakshinamoorthi, B. M., Chandrasekaran, R., Muthusamy, S., Ramamurthy, D., & Balasundaram, S. (2023). Integrating eco-technological approach for textile dye effluent treatment and carbon dioxide capturing from unicellular microalga Chlorella vulgaris RDS03: a synergistic method. International Journal of Phytoremediation, 25(4), 466-482.
- Tunca, H., Doğru, A., Köçkar, F., Önem, B. & Sevindik, T. O. (2020). Evaluation of Azadirachtin on Arthrospira plantensis Gomont growth parameters and antioxidant enzymes. Annales de Limnologie-International Journal of Limnology, 56, 1-8.
- Tunca, H., Özpınar, S. Ç., Tekbaba, A. G., Sevindik, T. O., Günsel, A., Bilgiçli, A. T., & Yaraşır, M. N. (2022). Algaecidal and oxidative effects of metal-free phthalocyanine beta tetra-substituted with sodium 2-mercaptoethanesulfonate. Turkish Journal of Chemistry, 46 (2), 367-377.
- Valentine, J. S., Wertz, D. L., Ltons, T. J., Liou, L. L., Goto, J. J. & Gralla, E. B. (1998). The dark side of dioxygen biochemistry. Current Opinion In Chemical Biology, 2, 253-262.
- Vervliet-Scheebaum, M., Alain Straus, A., Horst Tremp, H., Hamer, M., Maund, S. J., Edgar Wagner E & Schulz R (2010). A microcosm system to evaluate the toxicity of the triazine herbicide simazine on aquatic macrophytes. Environmental Pollution 158, 615–623.
- Walsh, G. E. (1978). Toxic Effects of Pollutants on Plankton. Principles of Ecotoxicology. 257-274, USA.
- Wang, H., & Ki, J. S. (2020). Molecular identification, differential expression and protective roles of iron/manganese superoxide dismutases in the green algae Closterium ehrenbergii against metal stress. European Journal of Protistology, 74, 125689.
- Wang, L., Riaz, M., Song, B., Song, X., Huang, W., Bai, X., & Zhao, X. (2022). Study on phytotoxicity evaluation and physiological properties of nicosulfuron on sugar beet (Beta vulgaris L.). Frontiers in Plant Science, 13, 998867.
- Wang, S. Y., Jiao, H., Faust, M. (1991). Changes in ascorbate, glutathione, and related enzyme activity during thidiazuron-induced bud break of apple. Plant Physiology 82: 231-236.
- Wang, Z. H., Xie, J., Jiang, S., Shi, J., Liu, Y. & Gong, W. (2012). Effects of commercial cypermethrin on the growth of Scenedesmus obliquus and its physiochemical responses. China Environmental Science 32 (4): 659-665.
- Weimberg, R. (1987). Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiologia Plantarum 70: 381-388.
- Wu, S., Zhang, H. & Qiu, L. (2014). Toxicological Responses of Chlorella vulgaris to Dichloromethane and Dichloroethane. Environmental Engineering Science 31: 1.
- Wu, Z. X., Xu, N. W., Yang, M., Li, X. L., Han, J. L., Lin, X. H., ... & Wang, J. (2022). Responses of photosynthesis, antioxidant enzymes, and related gene expression to nicosulfuron stress in sweet maize (Zea mays L.). Environmental Science and Pollution Research, 29(25), 37248-37265.
- Xu, L., Zhao, Z., Yan, Z., Zhou, G., Zhang, W., Wang, Y., & Li, X. (2022). Defense pathways of Chlamydomonas reinhardtii under silver nanoparticle stress: Extracellular biosorption, internalization and antioxidant genes. Chemosphere, 291, 132764.
- Yang, Y., Fan, X., Zhang, J., Qiao, S., Wang, X., Zhang, X., ... & Hou, J. (2022). A critical review on the interaction of iron-based nanoparticles with blue-green algae and their metabolites: From mechanisms to applications. Algal Research, 64, 102670.