Chemia Naissensis Volume 8, No.1 (2025) (стр. 36-51)
АУТОР(И) / AUTHOR(S): Nikola Stanković
, Ivana Kostić Kokić
, Tatjana Anđelković
, Monika Dudić
and Tamara Petronijević
Download Full Pdf 
DOI: https://doi.org/10.46793/ChemN8.1.36S
САЖЕТАК / ABSTRACT:
Microcystin-RR (MC-RR), a common cyanotoxin frequently detected in freshwater ecosystems, can influence phytoplankton dynamics by altering the growth patterns of coexisting species. While a large body of work has examined the allelopathic effects of microcystin-RR (MC-LR) and other microcystin variants, there are relatively few studies that specifically address the impact of pure MC-RR on phytoplankton species, particularly those that themselves produce this toxin, under environmentally relevant concentrations. This study investigated the effects of an environmentally relevant concentrations of MC-RR (1, 5, and 10 µg L⁻¹) on the growth of five phytoplankton species: three cyanobacteria (Trichormus variabilis, Nostoc sp., Microcystis sp.) and two green microalgae (Chlorella sp., Scenedesmus sp.), under laboratory conditions. Growth responses were monitored spectrophotometrically to determine chlorophyll a concentration over a 14-day period. Additionally, MC-RR was identified and quantified in the treated cyanobacterial cultures using the HPLC-DAD technique. The results demonstrated species-specific responses. MC-RR exhibited a stimulatory effect on both green algae species. In contrast, T. variabilis showed progressive growth inhibition, which became statistically significant after day 5. Nostoc sp. displayed slight, non- significant inhibition, while Microcystis sp. showed tolerance to MC-RR exposure. These findings demonstrate the allelopathic potential of MC-RR, with species-specific effects on growth that reflect differential sensitivity among phytoplankton taxa. The results underscore the ecological relevance of this toxin in shaping phytoplankton community structure and species interactions in freshwater ecosystems.
КЉУЧНЕ РЕЧИ / KEYWORDS:
cyanotoxin, microcystin-RR, allelophathy, phytoplankton, microbial community
ПРОЈЕКАТ/ ACKNOWLEDGEMENT:
This study was performed within the research program – Contract No. 451-03-136/2025- 03/200124.
ЛИТЕРАТУРА / REFERENCES:
- Alexova, R., Haynes, P. A., Ferrari, B. C., & Neilan, B. A. (2011). Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa. Molecular & Cellular Proteomics, 10(9), M110.003749. https://doi.org/10.1074/mcp.M110.003749
- Babica, P., Hilscherová, K., Bártová, K., Bláha, L., & Maršálek, B. (2007). Effects of dissolved microcystins on growth of planktonic photoautotrophs. Phycologia, 46(2), 137–142. https://doi.org/10.2216/06-24.1
- Campos, A., Araújo, P., Pinheiro, C., Azevedo, J., Osório, H., & Vasconcelos, V. (2013). Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicology and Environmental Safety, 94, 45–53. https://doi.org/10.1016/j.ecoenv.2013.04.019
- Christiansen, G., Fastner, J., Erhard, M., Börner, T., & Dittmann, E. (2003). Microcystin biosynthesis in Planktothrix: Genes, evolution, and manipulation. Journal of Bacteriology, 185(2), 564–572. https://doi.org/10.1128/jb.185.2.564-572.2003
- Cheng, F., & Cheng, Z. (2015). Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Frontiers in Plant Science, 6, 1020. https://doi.org/10.3389/fpls.2015.01020
- Díez-Quijada, L., Prieto, A. I., Guzmán-Guillén, R., Jos, A., & Cameán, A. M. (2019). Occurrence and toxicity of microcystin congeners other than MC-LR and MC-RR: A review. Food and Chemical Toxicology, 125, 106–132. https://doi.org/10.1016/j.fct.2018.12.042
- Díez-Quijada, L., Puerto, M., Gutiérrez-Praena, D., Llana-Ruiz-Cabello, M., Jos, A., & Cameán, M. (2019). Microcystin-RR: Occurrence, content in water and food, and toxicological studies — A review. Environmental Research, 168, 467–489. https://doi.org/10.1016/j.envres.2018.07.019
- Falkowski, P. G. (1994). The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynthesis Research, 39(3), 235–258. https://doi.org/10.1007/BF00014586
- Gan, N., Xiao, Y., Zhu, L., Wu, Z., Liu, J., Hu, C., & Song, L. (2012). The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environmental Microbiology, 14(3), 730–742. https://doi.org/10.1111/j.1462-2920.2011.02624.x
- Graham, L. E., Graham, J. M., & Wilcox, L. W. (2009). Algae. Pearson/Benjamin Cummings. Gross, E. M. (2003). Allelopathy of aquatic autotrophs. Critical Reviews in Plant Sciences, 22(3– 4), 313–339. https://doi.org/10.1080/713610859
- Greenstein, K. E., Zamyadi, A., Glover, C. M., Adams, C., Rosenfeldt, E., & Wert, E. C. (2020). Delayed release of intracellular microcystin following partial oxidation of cultured and naturally occurring cyanobacteria. Toxins, 12(5), Article 335. https://doi.org/10.3390/toxins12050335
- Hu, C., & Rzymski, P. (2019). Programmed cell death-like and accompanying release of microcystin in freshwater bloom-forming cyanobacterium Microcystis: From identification to ecological relevance. Toxins, 11(12), 706. https://doi.org/10.3390/toxins11120706
- Kaplan, A., Harel, M., Kaplan-Levy, R. N., Hadas, O., Sukenik, A., & Dittmann, E. (2012). The languages spoken in the water body (or the biological role of cyanobacterial toxins). Frontiers in Microbiology, 3, 138. https://doi.org/10.3389/fmicb.2012.00138
- Kosek, K., Polkowska, Ż., Żyszka, B., & Lipok, J. (2016). Phytoplankton communities of polar regions – Diversity depending on environmental conditions and chemical anthropopressure. Journal of Environmental Management, 171, 243–259. https://doi.org/10.1016/j.jenvman.2016.01.026
- Leão, P. N., Pereira, A. R., Liu, W., Ng, J., Pevzner, P. A., Dorrestein, P. C., König, G. M., Vasconcelos, V. M., & Gerwick, W. H. (2010). Synergistic allelochemicals from a freshwater cyanobacterium. Proceedings of the National Academy of Sciences of the United States of America, 107(25), 11183–11188. https://doi.org/10.1073/pnas.0914343107
- Li, H., Xie, P., Zhang, D., & Chen, J. (2009). The first study on the effects of microcystin-RR on gene expression profiles of antioxidant enzymes and heat shock protein-70 in Synechocystis sp. PCC 6803. Toxicon, 53(6), 595–601. https://doi.org/10.1016/j.toxicon.2008.11.005
- Li, J., Xiao, X., Xian, X., Li, S., Yu, X., & Zhang, X. (2023). Green algae outcompete cyanobacteria in a shallow lake, Longhu Lake. Water Supply, 23(7), 2649–2661. https://doi.org/10.2166/ws.2023.154
- Li, Z., Zheng, Y., Ma, H., & Cui, F. (2024). Microcystin-LR (MC-LR) inhibits green algae growth by regulating antioxidant and photosynthetic systems. Harmful Algae, 134, 102623. https://doi.org/10.1016/j.hal.2024.102623
- Litchman, E., de Tezanos Pinto, P., Edwards, K. F., Klausmeier, C. A., Kremer, C. T., & Thomas, K. (2015). Global biogeochemical impacts of phytoplankton: A trait-based perspective. Journal of Ecology, 103, 1384–1396. https://doi.org/10.1111/1365-2745.12438
- Martínez-Piernas, A. B., Badagian, N., Brena, B. M., Pérez-Parada, A., & García-Reyes, J. F. (2025). Identification and occurrence of microcystins in freshwaters and fish from a eutrophic dam through LC-HRMS. Science of the Total Environment, 959, 178230. https://doi.org/10.1016/j.scitotenv.2024.178230
- Mattson, M. P. (2008). Hormesis defined. Ageing Research Reviews, 7(1), 1–7. https://doi.org/10.1016/j.arr.2007.08.007
- Minasyan, A., Christophoridis, C., Wilson, A. E., Zervou, S.-K., Kaloudis, T., & Hiskia, A. (2018). Diversity of cyanobacteria and the presence of cyanotoxins in the epilimnion of Lake Yerevan (Armenia). Toxicon, 150, 28–38. https://doi.org/10.1016/j.toxicon.2018.04.003
- Omidi, A., Pflugmacher, S., Kaplan, A., Kim, Y. J., & Esterhuizen, M. (2021). Reviewing interspecies interactions as a driving force affecting the community structure in lakes via cyanotoxins. Microorganisms, 9(8), 1583. https://doi.org/10.3390/microorganisms9081583
- Paerl, H. W., & Otten, T. G. (2013). Harmful cyanobacterial blooms: Causes, consequences, and controls. Microbial Ecology, 65, 995–1010. https://doi.org/10.1007/s00248-012-0159-y
- Perron, M.-C., Qiu, B., Boucher, N., Bellemare, F., & Juneau, P. (2012). Use of chlorophyll a fluorescence to detect the effect of microcystins on photosynthesis and photosystem II energy fluxes of green algae. Toxicon, 59(5), 567–577. https://doi.org/10.1016/j.toxicon.2011.12.005
- Polyak, Y. M., & Sukharevich, V. I. (2025). Allelopathic properties of cyanobacteria (review). Inland Water Biology, 18, 565–574. https://doi.org/10.1134/S1995082925600358
- Revillini, D., David, A. S., Reyes, A. L., Knecht, L. D., Vigo, C., Allen, P., Searcy, C. A., & Afkhami, M. E. (2023). Allelopathy-selected microbiomes mitigate chemical inhibition of plant performance. New Phytologist, 240(5), 2007–2019. https://doi.org/10.1111/nph.19249
- Saleem, A., Anwar, S., Saud, S., et al. (2025). Cyanobacteria diversity and ecological roles: Insights into cyanobacterial adaptations and environmental implications. Journal of Umm Al-Qura University Applied Sciences. https://doi.org/10.1007/s43994-025-00261-2
- Schirrmeister, B. E., Gugger, M., & Donoghue, P. C. J. (2015). Cyanobacteria and the Great Oxidation Event: Evidence from genes and fossils. Palaeontology, 58, 769–785. https://doi.org/10.1111/pala.12178
- Sedmak, B., & Eleršek, T. (2005). Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microbial Ecology, 50(2), 298–305. https://doi.org/10.1007/s00248-004-0189-1
- Srimongkol, P., Sangtanoo, P., Songserm, P., Watsuntorn, W., & Karnchanatat, A. (2022). Microalgae-based wastewater treatment for developing economic and environmental sustainability: Current status and future prospects. Frontiers in Bioengineering and Biotechnology, 10, 904046. https://doi.org/10.3389/fbioe.2022.904046
- Stankovic, R. N. (2020). Phytoplankton influence on benthic macroinvertebrates of freshwater ecosystems in multistress conditions: laboratory testing of the toxic effect of cyanobacteria and green microalgae on individuals of the species Chironomus riparius. Doctoral dissertation. University of Niš, Faculty of Mathematics and Natural Siences
- Stanković, N., Jovanović, B., Kokić, I. K., Piperac, M. S., Simeunović, J., Jakimov, D., Dimkić, I., & Milošević, D. (2022). Toxic effects of a cyanobacterial strain on Chironomus riparius larvae in a multistress environment. Aquatic Toxicology, 253, 106321.
- Suikkanen, S., Fistarol, G. O., & Granéli, E. (2004). Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. Journal of Experimental Marine Biology and Ecology, 308(1), 85–101. https://doi.org/10.1016/j.jembe.2004.02.012
- Teneva, I., Velikova, V., Belkinova, D., Moten, D., & Dzhambazov, B. (2023). Allelopathic potential of the cyanotoxins microcystin-LR and cylindrospermopsin on green algae. Plants, 12(6), 1403. https://doi.org/10.3390/plants12061403
- Tonietto, Â., Petriz, B. A., Araújo, W. C., Mehta, Â., Magalhães, B. S., & Franco, O. L. (2012). Comparative proteomics between natural Microcystis isolates with a focus on microcystin synthesis. Proteome Science, 10, Article 38. https://doi.org/10.1186/1477-5956-10-38
- Wei, N., Hu, L., Song, L., & Gan, N. (2016). Microcystin-Bound Protein Patterns in Different Cultures of Microcystis aeruginosa and Field Samples. Toxins, 8(10), 293. https://doi.org/10.3390/toxins8100293
- Willis, R. J. (2007). The history of allelopathy. Springer. https://doi.org/10.1007/978-1-4020-4093-1
- Wei, N., Hu, C., Dittmann, E., Song, L., & Gan, N. (2024). The biological functions of microcystins. Water Research, 262, 122119. https://doi.org/10.1016/j.watres.2024.122119
- Whitton, B. A., & Potts, M. (2012). Introduction to the cyanobacteria. In B. A. Whitton (Ed.), Ecology of Cyanobacteria II (pp. 1–13). Springer, Dordrecht. https://doi.org/10.1007/978-94-007- 3855-3_1
- Wood, S. A., Puddick, J., Hawes, I., Steiner, K., Dietrich, D. R., & Hamilton, D. P. (2021). Variability in microcystin quotas during a Microcystis bloom in a eutrophic lake. PLoS ONE, 16(7), e0254967. https://doi.org/10.1371/journal.pone.0254967
- Yarnold, J., Karan, H., Oey, M., & Hankamer, B. (2019). Microalgal aquafeeds as part of a circular bioeconomy. Trends in Plant Science, 24(10), 959–970. https://doi.org/10.1016/j.tplants.2019.06.005
- Zanchett, G., & Oliveira-Filho, E. C. (2013). Cyanobacteria and cyanotoxins: From impacts on aquatic ecosystems and human health to anticarcinogenic effects. Toxins (Basel), 5(10), 1896- 1917. https://doi.org/10.3390/toxins5101896
- Zilliges, Y., Kehr, J.-C., Mikkat, S., Bouchard, J., de Marsac, N. T., Börner, T., … & Dittmann, (2011). The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress. Science, 334(6062), 81–85. https://doi.org/10.1126/science.1208583
- Žegura, B., Štraser, A., & Filipič, M. (2011). Genotoxicity and potential carcinogenicity of cyanobacterial toxins – A review. Mutation Research/Reviews in Mutation Research, 727(1–2), 16–41. https://doi.org/10.1016/j.mrrev.2011.01.002
- Śliwińska-Wilczewska, S., Wiśniewska, K., Budzałek, G., & Konarzewska, Z. (2022). Phenomenon of allelopathy in cyanobacteria. In Cyanobacterial Biology in Freshwater and Marine Systems (pp. —). Springer. https://doi.org/10.1007/978-981-16-4873-1_11
- Śliwińska-Wilczewska, S., Wiśniewska, K., Konarzewska, Z., Cieszyńska, A., Barreiro Felpeto, A., Lewandowska, A. U., & Latała, A. (2021). The current state of knowledge on taxonomy, modulating factors, ecological roles, and mode of action of phytoplankton allelochemicals. Science of the Total Environment, 773, 145681. https://doi.org/10.1016/j.scitotenv.2021.145681
