Effects of different phosphorus concentrations in medium on growth, biomass, total phenol contents, and evaluation of antioxidant properties in freshwater cyanobacteria Microcystis aeroginosa andAnabeana variabilis

Document Type : Research Paper

Authors

1 Ph. D. student, Department of Natural Resources, University of Isfahan Technology, Isfahan, Iran

2 Associate Professor, Department of Natural Resources, Isfahan University of Technology, Isfahan, Iran

3 Professor, Department of Natural Resources, Isfahan University of Technology, Isfahan, Iran

4 Associate Professor, Department of Pharmacy and Pharmaceutical Sciences, Isfahan University, Isfahan, Iran

10.22059/jfisheries.2023.356917.1375

Abstract

Phosphorus plays an important role in the growth of algae, production of fatty acids and metabolic processes such as energy transfer and photosynthesis. This study aimed to determine the effect of different phosphorus (P) concentrations on the growth, biomass, phenolic content and antioxidant properties of Microcystis aeroginosa and Anabeana variabilis. After identifying and isolation the desired cyanobacteria, in a completely randomized experimental design was conducted with four different concentrations of Phosphorus in the media, including zero, 0.5, 64 and 256 µgP/L, each in triplicates, using BG11 medium for a 10- day period culture. The average cell density in the treatments of 0 (control), 0.5, 64 and 256 µg/L of P for M. aeroginosa were recorded at 5.2×105, 6.4×105, 10.6×105 and 11.3×105 cells/mL, respectively, for A. variabilis were 2.8×105, 3.4×105, 7.7×105 and 1.4×105 cells/mL, respectively. The amount of total phenolic for M. aeroginosa were 0.5, 1.5, 5.12 and 7.75 mg gallic acid/ DW and for A. variabilis were 4.12, 4.9, 9 and 66.0 mg gallic acid/DW. The DPPH free radical inhibition percentage for M. aeroginosa were equal to 20.51, 22, 23 and 39.23% and for A. variabilis, 25.9, 32.56, 45.12 and 34.1% were calculated. The results showed that the highest growth, photosynthetic pigments and total phenolic as well as antioxidant content were obtained for M. aeroginosa at a concentration of 256 µg/L of P and for A. variabilis at concentration of 64 µg/L of P. Therefore, it can be concluded that the requirement of P in algae is different according to the species, so that each species shows the highest growth rate and other biological activities at a certain concentration of P. Also, understanding the growth of cyanobacteria in relation to the concentration of nutrients in which lead to their bloom is importance for their management of natural water resources, especially fresh and drink waters.

Keywords

Main Subjects

References

Andrade, M.A., Lima, V., Sanches-Silva, A., Vilarinho, F., Castilho, M.C., Khwaldia, K., Ramos, F., 2019. Pomegranate and grape by-products and their active compounds: Are they a valuable source for food applications. Trends in Food Science and Technology 86(1), 68-84, DOI: org/10.1016/j.tifs.2019.02.010
Aslan, S., Kapdan, I.K., 2006. Batch kinetics of nitrogen and phosphorus removal from synthetic wastewater by algae. Journal of Ecological Engineering 28(1), 64-70, DOI: 10.1016/j.ecoleng.2006.04.003
Atiku, A., Mohamed, R.M.S.R., Al-Gheethi, A.A., Wurochekke, A.A., Kassim, A.H., 2016. Harvesting microalgae biomass from the phyco remediation process of grey water. Journal of Environmental Science and Pollution Research 23(2), 24624-24641, DOI: 10.1007/s11356-016-7456-9
Barsanti, L., Gualtieri, P. 2006. Algae: Anatomy, Biochemistry, and Biotechnology, CRC Press, Taylor and Francis Group.320 pp, DOI: 10.1201/b16544
Blaise, W.L., Owen, K.D., Stephen, B., Anthony, D., Thomas, D., 2009. Antioxidant activity of Sonoran Desert bee pollen. Journal of Food Chemistry 115, 1299 – 1305, DOI: 10.1016/j.foodchem.2009.01.055
Beardall, J., Berman, T., Heraud, P., Kadiri, M.O., Light, B.R et al., 2001. A comparison of methods for detection of phosphate limitation in microalgae. Journal of Aquatic Sciences 63, 107-121, DOI: 10.1007/PL00001342
Bellinger, G.E. & Sigee, D.C., 2015. Freshwater Algae: Identification, Enumeration and Use as Bioindicators. (2ndEds). Freshwater Ecology p. 290, DOI:10.1002/9781118917152
Borodin, V.B., Tsygankov, A.A., Rao, K.K., Hall, D.O., 2000. Hydrogen production by Anabaena variabilis PK84 under simulated outdoor conditions. Journal of Biotechnology and Bioengineering 69(5), 478-485, DOI:10.1002/1097-0290(20000905)69:5%3C478::AID-BIT2%3E3.0.CO;2-L
Chaffin, J.D., Bridgeman, T.B., Heckathorn, S.A., Mishra, S., 2011. Assessment of Microcystis growth rate potential and nutrient status across a trophic gradient in western Lake Erie. Journal of Great Lakes Research 37(1), 92–100, DOI:10.1016/j.jglr.2010.11.016
Chu, Z., Jin, X., Yang, B., Zeng, Q., 2007. Buoyancy regulation of Microcystis flosaquae during phosphorus-limited and nitrogen-limited growth. Journal of Plankton Research 29(9), 739-745, DOI: 10.1093/plankt/fbm054
Custódio, L., Justo, T., Silvestre, L., Barradas, A., Duarte, C.V., Pereira, H., Varela, J., 2011. Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Journal of Food Chemistry 131, 134–140,   DOI: 10.1016/j.foodchem.2011.08.047
Dignum, M., Matthijs, H.C.P., Pel, R., Laanbroek, H.J. Mur, L.R., 2005. Nutrient Limitation of Freshwater Cyanobacteria. In Harmful Cyanobacteria; Huisman J. Matthijs HCP. (Eds). Springer: Dordrecht, the Netherlands. Pp. 65–86,   DOI: 10.1007/1-4020-3022-3_4
Chaffin, J.A., Watson, S.B., McCauley, E., 2001. Predicting cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58(10), 1905–1908, DOI: 10.1139/cjfas-58-10-1905
El-Sheek, M., Rady, A., 1995. Effect of phosphorus starvation on growth, photosynthesis and some metabolic processes in the unicellular green alga Chlorella kessleri. Phyton 35, 139-151.
Farhadian, O., Fallahi, M., Mahboubi Soofiani, N., 2013. Effects of different phosphorus concentrations on biomass and growth in green microalgae Chlorococcum sp. Journal of Plant Research 27(3), 478-489. (in Prsian), DOR: 20.1001.1.23832592.1393.27.3.14.6
Fernández-Juárez, V., Bennasar-Figueras, A., Sureda-Gomila, A., Ramis-Munar, G., Agawin, S.R.N., 2020. Differential effects of varying concentrations of phosphorus, iron, and nitrogen in N2-fixing Cyanobacteria. Frontiers in Microbiology 11, 541558. DOI: 10.3389/fmicb.2020.541558
Galhano, V., Figueiredo, D.R., 2011. Morphological, biochemical and molecular characterization of Anabaena, Aphanizomenon and Nostoc strains (Cyanobacteria, Nostocales) isolated from Portuguese freshwater habitats. Journal of Hydrobiologia 663, 187-203, DOI: 10.1007/s10750-010-0572-5
Ghaffar, S., Stevenson, R.J., Khan, Z., 2017. Effect of phosphorus stress on Microcystis aeroginosa growth and phosphorus uptake. PLoS ONE 12(3), e0174349, DOI: 10.1371/journal.pone.0174349
Goiris, K., Muylaert, K., Fraeye, I., Foubert, I., De Brabanter, J., De Cooman, L., 2012. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. Journal of Applied Phycology 24, 1477–1486, DOI: 10.1007/s10811-012-9804-6
Goiris, K., Van Colen, W., Wilches, I., Tamariz, F.L., De Cooman, L., Muylaert, K., 2015. Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Research (7), 51-57, DOI: 10.1016/j.algal.2014.12.002
Gorji, M.N., Modarresi, M., Keysami, M., Jamali, F., 2016. Optimization of BG-11 culture medium for increasing antifungal activity of Cyanobacterium sp. PGU1 against some plant pathogenic fungi. Biological Control of Pests and Plant Diseases 5(1), 49–58, DOI: 10.22059/jbioc.2016.58604
Hajimahmoodi, M., Faramarzi, M.A., Mohammadi, N., Soltani, N., Oveisi, M.R., Nafissi-Varcheh, N., 2010. Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. Journal of Applied Phycology 22, 43-50, DOI:10.1007/s10811-009-9424-y
Hamouda, R.A.E., Abou-El-Souod, G.W., 2018. Influence of various concentrations of phosphorus on the antibacterial, antioxidant and bioactive components of green microalgae Scenedesmus obliquus. International Journal of Pharmacology 14(1), 99-107, DOI: 10.3923/ijp.2018.99.107
Heydary, N., Nejatkhah, P., Ramezanpour, Z., Sabahi, M., 2009. Effects of different concentrations of phosphorous on the growth of the Cyanobacteria Jaaginema sp. and its toxic effects on aquatic organisms. Journal of Islamic Azad University of Veterinary 4(2), 15-20. (in Persian).
Jacobson, L., Halmann, M., 1982. Polyphosphate metabolism in the blue-green alga Microcystis aeruginosa. Journal of Plankton Research 4(3), 481-488. DOI: 10.1093/plankt/4.3.481.
Janes van Vuuren, S., Taylor, J., Gerber, A., Van Ginkel, C., 2006. Easy identification of the most common freshwater algae. A guide for the identification of microscopic algae in South Africean freshwater. ISBN 0-621-35471-6.
Jensen, A., 1978. Chlorophylls and carotenoids. In: Hellebust JA, Craige IS. (ed). Hand book of Phycological Methods.
Physiological and Biochemical Methods. Cambridge: Cambridge University Press. p. 59-70.
Khajehpour, F., Hosseini, A., Ghorbami, R., Shabanpour, B., 2016. Response of Nostoc calcicola to phosphorus of medium at different day of culture. Journal of Aquaculture Development 10(1), 43-51 (In Prsian), http://dorl.net/dor/20.1001.1.23223545.1395.10.1.7.7.
Kuda, T., Tsunekawa, M., Goto, H., Araki, Y., 2005. Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. Journal of Food Composition and Analysis 18(7), 625-633, DOI: 10.1016/j.jfca.2004.06.015.
Li, M., Shi, X., Guo, C., Lin, S., 2016. Phosphorus deficiency inhibits cell division but not growth in the dinoflagellate Amphidinium carterae. Frontiers in Microbiology 7, 826, DOI: 10.3389/fmicb.2016.00826.
Manivannan, K., Anantharaman, P., Balasubramanian, T., 2012. Evaluation of antioxidant properties of marine microalga Chlorella marina (Butcher, 1952). Asian Pacific Journal of Tropical Biomedicine 2, S342–S346, DOI: 10.1016/S2221-1691(12)60185-3.
Marker, A.F.H., 1972. The use of acetone and methanol in the estimation of chlorophyll in the presence of phaeophytin. Freshwater Biology 2, 361-385, DOI: 10.1111/j.1365-2427.1972.tb00377.x.
Martinez, M.E., Yang, J., Correa, G., 2000. Nitrogen and phosphorus removal from urban wastewater by the microalgae Scenedesmus obliqus. Bioresource Technology 73, 263-272, DOI: 10.1016/S0960-8524(99)00121-2.
Morone, J., Alfeus, A., Vasconcelos, V., Martins, R., 2019. Revealing the potential of cyanobacteria in cosmetics and cosmeceuticals-A new bioactive approach. Algal Research 41, 101541, DOI: 10.1016/j.algal.2019.101541.
Mueller, S., Mitrovic, S.M., 2014. Phytoplankton co-limitation by nitrogen and phosphorus in a shallow reservoir: Progressing from the phosphorus limitation paradigm. Hydrobiologia744, 255–269, DOI: 10.1007/s10750-014-2082-3.
Nalewajko, C.P., Murphy, T., 2001.  Effects of temperature, and availability of nitrogen and phosphorus on the abundance of Anabaena and Microcystis in Lake Biwa, Japan: an experimental approach. Journal of Limnology 2, 45-48, DOI: 10.1007/s102010170015.
Olasehinde, T.A., Odjadjare, E.C., Mabinya, L.V., Olaniran, A.O., Okoh, A.I., 2019. Chlorella sorokiniana and Chlorella minutissima exhibit antioxidant potentials, inhibit. Electron. Journal of Biotechnology 40, 1–9, DOI: 10.1016/j.ejbt.2019.03.008.
Omori, M., Ikeda, T., 1984. Methods in Marine Zooplankton Ecology. (1st Eds). Wiley, J. & Inc, S. New York, USA. 332 p.
Ota, S., Yoshihara, M., Yamazaki, T., Takeshita,. T., Hirata, A., Konomi, M., Oshima, K., Hattori, M., Bisova, K., Zachleder, V. et al., 2016. Deciphering the relationship among phosphate dynamics, electron-dense body and lipid accumulation in the green alga Parachlorella kessleri. Scientific Reports 6, 25731.
Paerl, H.W., Xu, H., McCarthy, M.J., Zhu, G., Qin, B., Li, Y., Gardner, W.S., 2011. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): The need for a dual nutrient (N & P) management strategy. Water Research 45, 1973–1983, DOI: 10.1016/j.watres.2010.09.018
Prairie, Y.T., Duarte, C. M., Kalff, J. 1989. Unifying nutrient chlorophyll relationship in lakes. Canadian Journal of Fisheries and Aquatic Science 46, 1176-1182, DOI: 10.1139/f89-153
Procházková, G., Brányiková, I., Zachleder, V., Brányik, T., 2013. Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. Journal of Applied Phycology 26, 1359–1377, DOI: 10.1007%2Fs10811-013-0154-9
Rabouille, S., Salencon, M.J., 2005. Functional analysis of Microcystis vertical migration: a dynamic model as a prospecting tool. II. Influence of mixing, thermal stratification and colony diameter on biomass production. Aquatic Microbial Ecology 39(3), 281–292, DOI: 10.3354/ame039281
Radkova, R., Stefanova, K., Uzunov, B., Gärtner, G., Stoyneva-Gärtner, M., 2020. Morphological and molecular identification of microcystin-producing Cyanobacteria in nine shallow Bulgarian water bodies. Journal of Toxins 12(39), 1-24, DOI: 10.3390/toxins12010039
Rico, M., 2013. Ló pez A, Santana-Casiano JM, Gonzá lez JM, Gonzá lez-Dá vila M. Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress. Limnology and Oceanography 58, 144–152, DOI: 10.4319/lo.2013.58.1.0144
Rippka, R., 1988. Isolation and purification of Cyanobacteria. Methods in Enzymology 167, 3-27, DOI: 10.1016/0076-6879(88)67004-2
Safari, M., Ahmadi-Asbechin, S., Soltani, N., 2015. In vitro assessment of antimicrobial activity from aqueous and methanolic extracts of some species of cyanobacteria. Biological Journal of Microorganism 14, 111-130, DOI: 10.5281/zenodo.3463632.
Sarkheil, M., Ameri, M., Safari, O., 2021. Application of alginate-immobilized microalgae beads as biosorbent for removal of total ammonia and phosphorus from water of African cichlid (Labidochromis lividus) recirculating aquaculture system. Environmental Science and Pollution Research 29(8), 11432-11444, DOI: 10.1007/s11356-021-16564-w.
Schachtman, P., Reid, R., Ayling, S., 1998. Phosphorus uptake by plants: from soil to cell. Journal of Plant Physiology 116, 447-453, DOI: 10.1104/pp.116.2.447
Singh, R., Parihar, P., Singh, M,. Bajguz, A., Kumar, J., Singh, S., Singh, V.P., Prasad. S.M., 2017. Uncovering potential applications of Cyanobacteria and algal metabolites in biology, agriculture and medicine: Current status and future prospects. Front Microbiology 8, 515, DOI: 10.3389/fmicb.2017.00515
Smith, S.V., 1984. Phosphorus versus nitrogen limitation in the marine environment. Limnology and Oceanography 29, 1149-1160, DOI; 10.4319/lo.1984.29.6.1149
Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G., 1971. Purification and properties of unicellular blue- green algae (order Chroococcales). Bacteriological Reviews 35, 171-205,  DOI: 10.1128/br.35.2.171-205.1971
Stratil, P., Klejdus, B., Kubáň, V., 2006. Determination of Total Content of phenolic compounds and their antioxidant activity in vegetables evaluation of spectrophotometric methods. Journal of Agricultural and Food Chemistry 54(3), 607-616, DOI: 10.1021/jf052334j
Tsukada, H., Tsujimura, S., Nakahara, H., 2006. Effect of nutrient availability on the C, N, and P elemental ratios in the cyanobacterium Microcystis aeruginosa. Limnology 7(3), 185-192, DOI: 10.1007/s10201-006-0188-7
Verspagen, J.M., Snelder,E.O., Visser, P.M., Huisman, J., Mur, L.R. Ibelings, B.W., 2004. Recruitment of benthic Microcystis (Cyanophyceae) to the water column: internal buoyancy changes or resuspension. Journal of Phycology 40(2), 260-270, DOI: 10.1111/j.1529-8817.2004.03174.x
Widjaja, A., Chien, C.C., Ju, Y.H., 2009. Study of increasing lipid production from fresh water microalgae Chlorella vulgaris. Journal of the Taiwan Institute of Chemical Engineers 40, 13-20, DOI: 10.1016/j.jtice.2008.07.007
Xin, L., Hong-ying, H., Ke, G., Ying-xue, S., 2010. Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresource Technology 101, 5494-5500, DOI: 10.1016/j.biortech.2010.02.016
Xiong, J., Kurade, M.B., Kim, J.R., Roh, H., Jeon, B., 2017. Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. Journal of Hazardous Materials 323, 212-219, DOI: 10.1016/j.jhazmat.2016.04.073
Xu, H., Paerl, H.W., Qin, B., Zhu, G., Gao, G., 2010. Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography 55, 420–432, DOI: 10.4319/lo.2010.55.1.0420
Yang, F.F,. Xiang, W., Li, T., Long,. L., 2018. Transcriptome analysis for phosphorus starvation-induced lipid accumulation in Scenedesmus sp. Scientific Reports 8, 1-11, DOI: 10.1038/s41598-018-34650-x
Yoon, J.H., Shin, J.H., Ahn, E.K,. Park, T.H., 2008. High cell density culture of Anabeana variabilis with controlled light intensity and nutrient supply. Journal of Microbiology and Biotechnology 18(5), 918-925,   DOI: 10.1038/s41598-018-34650-x
Zarinmehr, M.J., Farhadian, O., Peykan Heiraty, F., Keramat, J., 2021. Effect of different phosphorus concentrations on the growth rate and biochemical composition of golden-brown alga Isochrysis galbana. Journal of Plant process and function 9(36), 413-424. (in Persian). DOI: 10.3856/vol47-issue2-fulltext-17.
Zhang, W., Feng, Y., 2008. Characterization of nitrogen-fixing moderate halophilic cyanobacteria isolated from saline soils of Songnen Plain in China. Progress in Natural Science 18, 769-773, DOI: 10.1016/j.pnsc.2008.01.022
Journal of Fisheries
Volume 76, Issue 3
September 2023
Pages 357-376

Files

Share

How to cite

Statistics