The evaluation of the growth performance of a cyanobacterial isolate Phormidium lucidum (Kützing ex Gomont 1892) grown under different environmental conditions and its use as a dietary source for Daphnia magna (Straus 1820)

The evaluation of the growth performance of a cyanobacterial isolate Phormidium lucidum (Kützing ex Gomont 1892) grown under different environmental conditions and its use as a dietary source for Daphnia magna (Straus 1820)

This study presents the effect of cyanobacterium isolated from Bolluk Lake (Konya, Türkiye) which is a saline lake on the growth performance of Daphnia magna. Isolated cyanobacteria species were identified as Phormidium lucidum according to its 16S rDNA sequences. The effects of different growth conditions including pH (7.18, 8.15, 9.17 and 10.26), light intensity (1200, 2400, 3600 and 4800 lux), temperature (10, 20, 25 and 30°C) and nitrogen concentrations (0.25, 0.5, 1.0 and 1.5 g/L) on P. lucidum was studied. Effects of each environmental factor on biochemical composition (total protein, total lipid and chlorophyll-a concentration) of P. lucidum were also studied. The optimum growth conditions were found as pH 7.18, ambient temperature 20°C, nitrogen 0.25 g/L and light intensity 3600 lux, after a 2-week incubation period. The effects of various mixtures of the cyanobacteria and Chlorella vulgaris which is a common feed for Daphniids were also evaluated for their effects on the growth rates of D. magna. The best growth rate for D. magna was obtained in the medium containing 100% P. lucidum at the end of the 13ᵗ ͪ day.

___

  • Hitzfeld, B.C., Hoeger, S.J., Dietrich, D.R., Cyanobacterial toxins: removal during drinking water treatment and human risk assessment. Environ Health Perspect, 108(1) (2000), 113-122. https://doi.org/10.1289%2Fehp.00108s1113
  • Sukenik, A., Zohary, T., Padisak, J., Cyanoprokaryota and other prokaryotic algae, In: Likens, G.E., Editor. Encyclopedia of Inland Waters, Academic Press, (2009), 138-148.
  • Amarouche-Yala, S., Benouadah, A., Bentabet, A.E.O., Lopez-Garcia, P., Morphological and phylogenetic diversity of thermophilic cyanobacteria in Algerian hot spring. Extremophiles, 18(6) (2014), 1035-1047. https://doi.org/10.1007/s00792-014-0680-7
  • Moreira, C. Ramos, V. Azevedo, J., Vasconcelos, V., Methods to detect cyanobacteria and their toxins in the enviroment-mini rewiev. Applied Microbiology and Biotechnology, 98(19) (2014), 8073-8082. https://doi.org/10.1007/s00253-014-5951-9
  • Ikawa, M., Algal polyunsaturated fatty acid and effect on plankton ecology and other organisms. UNH Center for Freshwater Biology Research, 6(2) (2004), 17-44.
  • Converti, A., Casazza, A.A., Ortiz, E.Y., Perego, P., Borghi, M.D., Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chemical Engineering and Processing, 48(6) (2009), 1146–1151. https://doi.org/10.1016/j.cep.2009.03.006
  • Sharma, K.K., Schuhmann, H., Schenk, P.M., High lipid induction in microalgae for biodiesel production. Energies, 5(5) (2012), 1532-1553. https://doi.org/10.3390/en5051532
  • Kumar, B.R., Deviram, G., Mathimani, T., Duc, P.A., Pugazhendhi, A., Microalgae as rich source of polyunsaturated fatty acids. Biocatalysis and Agricultural Biotechnology, 17 (2019), 583–588. https://doi.org/10.1016/j.bcab.2019.01.017
  • Prihantini, N.B., Pertiwia, Z.D., Yuniatia, R., Sjamsuridzala, W., Putrikaa, A., The effect of temperature variation on the growth of Leptolyngbya (cyanobacteria) HS-16 and HS-36 to biomass weight in BG-11 medium. Biocatalysis and Agricultural Biotechnology, 19(6) (2019), 101-105. https://doi.org/10.1016/j.bcab.2019.101105
  • Hotos, G.N., Culture growth of the cyanobacterium Phormidium sp. in various salinity and light regimes and their influence on its phycocyanin and other pigments content. Journal of Marine Science and Engineering, 9(8) (2021), 798. https://doi.org/10.3390/jmse9080798
  • Yadav, G., Sekar, M., Kim, S.H., Geo, V.E., Bhatia, S.K., Sabirf, J.S.M., Chi, N.T.L., Brindhadevi, K., Pugazhendhi, A., Lipid content, biomass density, fatty acid as selection markers for evaluating the suitability of four fast growing cyanobacterial strains for biodiesel production. Bioresource Technology, 325 (2021), 124654. https://doi.org/10.1016/j.biortech.2020.124654
  • Mata, T.M., Martins, A.A., Sikdar, S., Costa, C.A.V., Sustainable considerations of biodiesel based on supply chain analysis. Clean Technologies and Environmental Policy, 13(5) (2011), 655-671. http://dx.doi.org/10.1007/s10098-010-0346-9
  • Griffiths, M.J., Hille, R.P.V., Harrison, S.T.L., Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applied Phycology, 24(5) (2012), 989–1001. http://dx.doi.org/10.1007/s10811-011-9723-y
  • Locke, A., Sprules, W.G., Effect of acidic pH and phytoplankton on survival and condition of Bosmina longirostris and Daphnia pulex. Hydrobiologia, 437 (2000), 187-196. https://doi.org/10.1023/A%3A1026563109217
  • Hansen, P.J., Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquatic Microbial Ecology, 28(3) (2002), 279-288. http://dx.doi.org/10.3354/ame028279" \t
  • Li, Y., Lin, Y., Loughlin, P.C., Chen, M., Optimization and effect of different culture conditions on growth of Halomicronema hongdechloris-a filamentous cyanobacterium containing chlorophyll-f. Plant Physiology, 5 (2014), 67. https://doi.org/10.3389/fpls.2014.00067
  • Rai, M.P., Gautom, T., Sharma, N., Effect of salinity, pH, light intensity on growth and lipid production of microalgae for bioenergy application. Online Journal of Biological Sciences, 15(4) (2015), 260-267. https://doi.org/10.3844/ojbsci.2015.260.267
  • Chandra, K., Rajashekhar, M., Effect of pH on freshwater cyanobacteria isolated from different habitats of Southern Karnatak. International Journal of Life Sciences and Technology, 9(7) (2016), 56-64. https://www.cabdirect.org/cabdirect/abstract/20173009127
  • Kumar, M., Kulshreshtha, J., Singh, G.P., Growth and biopigment accumulation of cyanobacterium spirulia platensis at different light intensitiies and temperature. Brazilian Journal of Microbiology, 42(3) (2011), 1128–1135. https://doi.org/10.1590%2FS1517-838220110003000034
  • Sanchez-Bayo, A., Morales, V., Rodriguez, R., Vicente, G., Bautista, L.F., Cultivation of microalgae and cyanobacteria: effect of operating conditions on growth and biomass composition. Molecules, 25(12) (2020), 2834. https://doi.org/10.3390/molecules25122834
  • Hotos, G.N., Antoniadis, T.I, The effect of colored and white light on growth and phycobiliproteins, chlorophyll and caretenoids content of the marine cyanobacteria Phormidium sp. and Cyanothece sp. in batch cultures. Life, 12(6) (2022), 837. https://doi.org/10.3390/life12060837
  • Mohanty, B. Majedi, S.M. Pavagadhi, S. Te, S.H. Boo, C.Y. Gin, K.Y-H., Swarup, S., Effect of light and temperature on the metabolic profiling of two habitat-dependent bloom-forming cyanobacteria. Metabolites, 12(5) (2022), 406. https://doi.org/10.3390/metabo12050406
  • Herrero, A., Muro-Pastor, A.M., Flores, E., Nitrogen control in cyanobacteria. Journal of Bacteriology, 183(2) (2001), 411-25. https://doi.org/10.1128/JB.183.2.411-425.2001
  • Wu, H., Miao, X., Biodiesel quality and biochemical changes of microalgae Chlorella pyrenoidosa and Scenedesmus obliquus in response to nitrate levels. Bioresource Technology, 170 (2014), 421-427. https://doi.org/10.1016/j.biortech.2014.08.017
  • Altındağ, A., Ergönül, M.B., Yigit, S., Baykan, Ö., The acute toxicity of lead nitrate on Daphnia magna Straus. African Journal of Biotechnology, 7(23) (2008), 4298-4300. https://doi.org/10.5897/AJB08.635
  • Yılmaz, H.K., Bilgüven, M., Ersoy, M., Su Piresinin (Daphnia magna S.) farklı besin ortamlarında verimliliği ve besinsel içeriği. Journal of Agricultural Faculty of Uludag University, 21(2) (2007), 65-74.
  • Turcihan, G., Isinibilir, M., Zeybek, Y.G., Eryalçın, K.M., Effect of different feeds on reproduction performance, nutritional components and fatty acid composition of cladocer water flea (Daphnia magna). Aquaculture Research, 53(6) (2022), 2420-2430. https://doi.org/10.1111/are.15759
  • Şanal, M., Köksal, G., Farklı besin ortamlarının Daphnia pulex’in üreme randımanı üzerine etkisi. Tarım Bilimleri Dergisi, 11(2) (2005), 173-177. https://doi.org/10.1501/Tarimbil_0000000414
  • Ölmez, M., Savaş, S., Güçlü, Z., Demir, O., Gümüş, E., Farklı ortamlarda üretilmiş Scenedesmus acuminatus alginin ve ekmek mayasının (Saccharomyces cerevisea) Daphnia magna’nın populasyon artışına etkisi. E.U. Journal of Fisheries and Aquatic Sciences, 26(1) (2009), 49-53.
  • Choi, J.Y., Kim, S.K., Chang, K.H., Kim, M.C., La, G.H., Joo, G.J., Jeong, K.S., Population growth of Cladoceran, Daphnia magna: a quantative analysis of the effect of different algal food. Quantitive Prey Contribution to Zooplankton, 9(4) (2014), e95591. https://doi.org/10.1371/journal.pone.0095591
  • Choi, J.Y., Kim, S.K., Chang, K.H., La, G.H., Kim, D. K., Jeong, K.Y. Park, M.S., Joo, G.J., Kim, H.W., Jeong, K.S., Effect of algal food quality on sexual reproduction of Daphnia magna. Ecology and Evolotion, 6(9) (2016), 2817-2832. https://doi.org/10.1002/ece3.2058
  • Akbulut, A., Dügel, M., Planktonic diatom assemblages and their relationship to environmental variables in lakes of Salt Lake basin (Central Anatolia-Turkey). Fresenius Environmental Bulletin, 17(2) (2008), 154-163.
  • Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., Stainer, R.Y., Genetic assignments, strains histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology, 111 (1979), 1-61. https://doi.org/10.1099/00221287-111-1-1
  • Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G., Purification and properties of unicellular blue-green algae (order Chlorococcales). Bacteriological Reviews, 35(2) (1971), 171–205. https://doi.org/10.1128%2Fbr.35.2.171-205.1971
  • Eryalçın, K.M., Effects of Different Commercial feeds and enrichments on biochemical composition and fatty acid profile of Rotifer (Brachionus plicatilis, Müller 1786) and Artemia franciscana. Turkish Journal of Fisheries and Aquatic Sciences, 18(2018), 81-90. http://dx.doi.org/10.4194/1303-2712-v18_1_09
  • Patel, V.K., Sundaram, S., Patel, A.K., Kalra, A., Characterization of seven species of cyanobacteria for high-quality biomass production. Arabian Journal of Science and Engineering, 43 (2017), 109-121. https://doi.org/10.1007/S13369-017-2666-0
  • Kersting, K., Leeuw-Leegwater, C.V.D., Effect of food concentration on the respiration of Daphnia magna. Hydrobiologia, 49 (2) (1976), 137-142. https://doi.org/10.1007/BF00772684
  • Cowgill, U.M., Emmel, H.W., Hopkins, D.L., Takahashi, I.T., Parker, W.M., Variation in chemical composition, reproductive success and body weight of Daphnia magna in relation to Diet. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 71(1) (1986), 79-99. https://doi.org/10.1002/iroh.19860710111
  • Tollrian R., Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. Journal of Plankton Research, 15(11) (1993), 1309–1318. https://doi.org/10.1093/PLANKT%2F15.11.1309
  • Wacker, A., Martin-Creuzburg, D., Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Functional Ecology, 21 (2007), 738–747. https://doi.org/10.1111/j.1365-2435.2007.01274.x
  • Stephenson, R.R., Watts, S.A., Chronic toxicity tests with Daphnia magna: the effects of different food and temperature regimes on survival, reproduction and growth. Environmental Pollution (Series A), 36(2) (1984), 95-107. https://doi.org/10.1016/0143--1471(84)90092-8
  • Lürling, M., Effects of microcystin-free and microcystin containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environmental Toxicology, 18(3) (2003), 202–210. https://doi.org/10.1002/tox.10115
  • Nandini, S., Sarma, S.S.S., Population growth of some genera of Cladocerans (Cladocera) in relation to algal food (Chlorella vulgaris) levels. Hydrobiologia, 491(1-3) (2003), 211-219. http://dx.doi.org/10.1023/A:1024410314313
  • Parsons, T.R., Strickland, J.D.H., Discussion of spectrophotometric determination of marine plant pigments with revised equations for ascertaining chlorophylls and carotenoids. Journal of Marine Research, 21(3) (1963), 115-163. https://doi.org/10.1016/0011-7471%2865%2990662-5
  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Andall, R.J., Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193(1) (1951), 265-275. http://dx.doi.org/10.1016/S0021-9258(19)52451-6
  • Bligh, E.G., Dyer, W.J., A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8) (1959), 911–917. https://doi.org/10.1139/o59-099
  • Adıgüzel, N., Byfield, A., Duman, H. ve Vural, M., Tuz Gölü ve Stepleri, In: Özhatay, N., Byfield, A., and Atay, S. Editors. Türkiye’nin 122 Önemli Bitki Alanı, WWF Türkiye (Doğal Hayatı Koruma Vakfı) Yayını, İstanbul, (2005) 289-292.
  • Ekim, T., Koyuncu, M., Vural, M., Duman, H., Aytaç, Z. ve Adıgüzel, N., Türkiye Bitkileri Kırmızı Kitabı (Pteridophyta and Spermatophyta), Türkiye Tabiatını Koruma Derneği ve Yüzüncü Yıl Üniversitesi Yayını, Ankara, 2000.
  • Pandey, J.P., Pathak, N., Tiwari, A., Standardization of pH and light intensity for the biomass production of Spirulina platensis. Journal of Algal Biomass Utilization, 1(2) (2010), 93-102.
  • Bhandari, R., Sharma, P.K., High-light induced changes on photosynthesis, pigments, sugars, lipids and antioxidant enzymes in freshwater (Nostoc spongiaeforme) and marine (Phormidium corium) cyanobacteria. Photochemistry and Photobiology, 82(3) (2006), 702-710. https://doi.org/10.1562/2005-09-20-ra-690
  • Solovchenko, A.E., Khozin-Goldberg, I., Didi-Cohen, S., Cohen, Z., Merzlyak, M.N., Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. Journal of Applied Phycology, 20(3) (2008), 245–251. http://dx.doi.org/10.1007/s10811-007-9233-0
  • Guedes, A.C., Meireles, L.A., Amaro, H.M., Malcata, F.X., Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to light intensity. Journal of American Oil Chemists Society, 87(7) (2010), 791–801. http://dx.doi.org/10.1007/s11746-010-1559-0" \t
  • Wahidin, S., Idris, A., Shaleh, S.R.M., The influence of light intensity and photoperiod on the growth and lipid content of microalgae Nannochloropsis sp. Bioresource Technology, 129 (2013), 7–11. https://doi.org/10.1016/j.biortech.2012.11.032
  • Jezberova, J., Komarkova, J., Morphometry and growth three Synechococcus-like picoplanktic cyanobacteria at different culture conditions. Hydrobiologia, 578(1) (2007), 17-27. http://dx.doi.org/10.1007/s10750-006-0429-0
  • Ma, R., Lu, F., Bi, Y., Hu, Z., Effects of light intensity and quality on phycobiliprotein accumulation in the cyanobacterium Nostoc sphaeroides Kützing. Biotechnol. Lett., 37(8) (2015), 1663-1669. https://doi.org/10.1007/s10529-015-1831-3" \t
  • Mandotra, S.K., Kumar, P., Suseela, M.R., Nayaka, S., Ramteke, P.W., Evaluation of fatty acid profile and biodiesel properties of microalga Scenedesmus abundans under the influence of phosphorus, pH and light intensities. Bioresource Technology, 201 (2016), 222–229. https://doi.org/10.1016/j.biortech.2015.11.042
  • Mondal, M., Ghosh, A., Tiwari, O.N., Gayen, K., Das, P., Mandal, M.K., Halder, G., Influence of carbon sources and light intensity on biomass and lipid production of Chlorella sorokiniana BTA 9031 isolated from coalfield under various nutritional modes. Energy Conversion and Management, 145 (2017), 247–254. http://dx.doi.org/10.1016/j.enconman.2017.05.001
  • Muhetaer, G., Asaeda, T., Jayasanka, S.M.D.H., Baniya, M.B. Abeynayaka, H.D.L., Rashid, M.H., Yan, H., Effects of light intensity and exposure period on the growth and stress responses of two cyanobacteria species: Pseudanabaena galeata and Microcystis aeruginosa. Water, 12(2) (2020), 407. https://doi.org/10.3390/w12020407
  • Health, M., Wood, S.A., Young, R.G., Ryan, K.G., The role of nitrogen and phosphorus in regulating Phormidium sp. (cyanobacteria) growth and anatoxin production. FEMS Microbiology Ecology, 92(3) (2016), fiw021. https://doi.org/10.1093/femsec/fiw021
  • Aboim, J.B., Oliveira, D.T., Mescouto, V.A., Reis, A.S., Filho, G.N.R., Santos, A.V., Xavier, L.P., Santos, A.S., Gonçalves, E.C., Nascimento, L.A.S., Optimization of light intensity and NaNO3 concentration in Amazon cyanobacteria cultivation to produce biodiesel. Molecules, 24(12) (2019), 2326. https://doi.org/10.3390/molecules24122326
  • Hong, S.J., Lee, C.G., Statistical optimization of culture media for production of phycobiliprotein by Synechocystis sp. PCC 6701. Biotechnology and Bioprocess Engineering, 13 (2008), 491-498. http://dx.doi.org/10.1007/s12257-008-0154-9
  • Crnkovic, C.M., May, D.S., Orjala, J., The impact of culture conditions on growth and metabolomic profiles of freshwater cyanobacteria. J. App.Phycol. 30(1) (2017), 375-384. https://doi.org/10.1007/s10811-017-1275-3
  • Khazi, M.I., Demirel, Z., Dalay, M.C., Evaluation of growth and phycobiliprotein composition of cyanobacteria isolates cultivated in different nitrogen sources. Journal of Applied Phycology, 30 (2018), 1513-1523. https://doi.org/10.1007/s10811-018-1398-1
  • Deng, X., Chen, B., Xue, C., Li, D., Hu, X., Gao, K., Biomass production and biochemical profiles of a freshwater microalga Chlorella kessleri in mixotrophic culture: effects of light intensity and photoperiodicity. Bioresource Technology on Science Direct, 273 (2019), 358-367. https://doi.org/10.1016/j.biortech.2018.11.032
  • Lürling, M., Eshetu, F., Daassen, E.J., Kosten, S., Huszar, V.L.M., Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology, 58(3) (2013), 552–559. https://doi.org/10.1111/j.1365-2427.2012.02866.x
  • Thomas, M.K., Litchman, E., Effect of temperature and nitrogen avaliability on the growth o invasive and native cyanobacteria. Hydrobiologia, 763(1) (2015), 357–369. http://dx.doi.org/10.1007/s10750-015-2390-2
  • Taipale, S.J., Brett, M.T., Pulkkinen, K., Kainz, M.J., The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction and lipid composition. FEMS Microbiology Ecology, 82(1) (2012), 50–62. https://doi.org/10.1111/j.1574-6941.2012.01406.x
  • Bednarska, A., Pietrzak, B., Pijanowska, J., Effect of poor manageability and low nutritional value of cyanobacteria on Daphnia magna life history performance. Journal of Plankton Research, 36(3) (2014), 838-847. http://dx.doi.org/10.1093/plankt/fbu009
  • Munirasu, S., Uthayakumar, V., Arunkumar, P., Ramasubramanian, V., The effect of different feeds such as Chlorella vulgaris, Azolla pinnata and yeast on the population growth of Daphnia magna commonly found in freshwater systems. International Journal of Fisheries and Aquatic Studies, 4(6) (2016), 5-10.
  • Yin, X.W., Lui, P.F., Zhu, P.P., Chen, X.X., Food selectivity of the herbivore Daphnia magna (Cladocera) and its impact on competition outcome between two freshwater green algae. Hydrobiologia, 655 (2010), 15–23. https://doi.org/10.1007/s10750-010-0399-0
  • Bednarska, A., Los, J., Dawıdowıcz, P., Temperature-dependent effect of filamentous cyanobacteria on Daphnia magna life history traits. Journal of Limnology, 70(2) (2011), 353-358. http://dx.doi.org/10.3274/JL11-70-2-19