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Can the presence of green microalgae reverse the allelopathic effects of the submerged macrophyte Egeria densa on the toxin-producing cyanobacterium Raphidiopsis raciborskii?

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Abstract

Investigations on the influence of green microalgae associated with cyanobacteria exposure to macrophytes and the production of cyanotoxins have not been previously explored. The effects of the presence of live plants and extracts of the Egeria densa, on the growth and saxitoxin production of Raphidiopsis raciborskii were investigated in the presence and absence of Chlorella vulgaris. The physical presence of the macrophyte reduced the biovolume of the cyanobacterium and its production of saxitoxins, while cultures exposed to aqueous extract had elevated saxitoxin levels. The green microalgae also increased the amount of cyanotoxins, especially when the macrophyte biomass was low. These findings suggest that E. densa can inhibit the growth of R. raciborskii and the production of cyanotoxins and that the presence of C. vulgaris can alter these processes.

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References

  • Aguilera, A., E. B. Gómez, J. Kaštovský, R. O. Echenique & G. L. Salerno, 2018. The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 57: 130–146.

    Article  CAS  Google Scholar 

  • Amorim, C. A., C. Ulisses & A. N. Moura, 2017. Biometric and physiological responses of Egeria densa Planch. cultivated with toxic and non-toxic strains of Microcystis. Aquatic Toxicology 191: 201–208.

    Article  CAS  PubMed  Google Scholar 

  • Antoniou, M. G., A. A. de La Cruz & D. D. Dionysiou &, 2005. Cyanotoxins: New Generation of Water Contaminants. Journal of Environmental Engineering 131: 1239–1243.

    Article  CAS  Google Scholar 

  • Antunes, J. T., P. N. Leão & V. M. Vasconcelos, 2015. Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology 6: 473.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ball, A. S., M. Williams, D. Vincent & J. Robinson, 2001. Algal growth control by a barley straw extract. Bioresource Technology 77: 177–181.

    Article  CAS  PubMed  Google Scholar 

  • Barbosa, V. V., J. S. Severiano, D. A. De Oliveira & J. E. L. Barbosa, 2020. Influence of submerged macrophytes on phosphorus in a eutrophic reservoir in a semiarid region. Journal of Limnology. https://doi.org/10.4081/jlimnol.2020.1931.

    Article  Google Scholar 

  • Berman-Frank, I., K. D. Bidle, L. Haramaty & P. G. Falkowski, 2004. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnology and Oceanography 49: 997–1005.

    Article  Google Scholar 

  • Bittencourt-Oliveira, M. C., V. Piccin-Santos, A. N. Moura, N. K. C. Aragão-Tavares & M. K. Cordeiro-Araújo, 2014. Cyanobacteria, microcystins and cylindrospermopsin in public drinking supply reservoirs of Brazil. Anais Da Academia Brasileira De Ciências 86: 297–310.

    Article  Google Scholar 

  • Bittencourt-Oliveira, M. C., M. K. Cordeiro-Araújo, M. A. Chia, J. D. T. Arruda-Neto, E. T. Oliveira & F. Santos, 2016. Lettuce irrigated with contaminated water: photosynthetic effects, antioxidative response and bio accumulation of microcystin congeners. Ecotoxicology and Environmental Safety 128: 83–90.

    Article  CAS  Google Scholar 

  • Campos, A., P. Araújo, C. Pinheiro, J. Azevedo, H. Osório & H. Vasconcelos, 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 Safe 94: 45–53.

    Article  CAS  Google Scholar 

  • Cao, Q., X. Wan, X. Shu & L. Xie, 2019. Bioaccumulation and detoxication of microcystin-LR in three submerged macrophytes: The important role of glutathione biosynthesis. Chemosphere 225: 935–942.

    Article  CAS  Google Scholar 

  • Carmichael, W. W. & G. L. Boyer, 2016. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 54: 194–212.

    Article  PubMed  Google Scholar 

  • Casali, S. P., A. C. Dos Santos, P. B. de Falco & M. D. C. Calijuri, 2017. Influence of environmental variables on saxitoxin yields by Cylindrospermopsis raciborskii in a mesotrophic subtropical reservoir. Journal Water Health 15: 509–518.

    Article  Google Scholar 

  • Chang, X., F. Eigemann & S. Hilt, 2012. Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae 19: 76–84.

    Article  CAS  Google Scholar 

  • Chen, J., H. Zhang, Z. Han, J. Ye & Z. Liu, 2012. The influence of aquatic macrophytes on Microcystis aeruginosa growth. Ecological Engineering 42: 130–133.

    Article  Google Scholar 

  • Chia, M. A. & M. C. Bittencourt-Oliveira, 2021. Allelopathic interactions between phytoplankton species alter toxin production, oxidative response, and nitrogen fixation. Hydrobiologia 19: 4623–4635.

    Article  Google Scholar 

  • Chia, M. A., J. G. Jankowiak, B. J. Kramer, J. A. Goleski, I. Huang, P. V. Zimba, M. Bittencourt-Oliveira & C. J. Gobler, 2018. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions. Harmful Algae 74: 67–77.

    Article  CAS  PubMed  Google Scholar 

  • Chia, M., B. Kramer, J. Jankowiak, M. C. Bittencourt-Oliveira & C. Gobler, 2019. The Individual and Combined Effects of the Cyanotoxins, Anatoxin-a and Microcystin-LR, on the Growth, Toxin Production, and Nitrogen Fixation of Prokaryotic and Eukaryotic. Algae Toxins 11: 43.

    Article  CAS  Google Scholar 

  • De Mendiburu, F, 2021.  Agricolae: Statistical Procedures for Agricultural Research. R Package version 1.3-1. https://CRAN.R-project.org/package=agricolae.

  • De Tezanos Pinto, P., L. Allende & I. O’Farrell, 2006. Influence of free-floating plants on the structure of a natural phytoplankton assemblage: an experimental approach. Journal of Plankton Research 29: 47–56.

    Article  Google Scholar 

  • Dong, J., K. Yang, S. Li, G. Li & L. Song, 2014. Submerged vegetation removal promotes shift of dominant phytoplankton functional groups in a eutrophic lake. Journal of Environmental Sciences 26: 1699–1707.

    Article  CAS  Google Scholar 

  • Espinosa-Rodríguez, C. A., L. Rivera-De la Parra, A. Martínez-Téllez, G. C. Gómez-Cabral, S. S. S. Sarma & S. Nandini, 2016. Allelopathic interactions between the macrophyte Egeria densa and plankton (alga, Scenedesmus acutus and cladocerans, Simocephalus spp.): a laboratory study. Journal of Limnology. https://doi.org/10.4081/jlimnol.2016.1397.

    Article  Google Scholar 

  • Fergola, S., M. Cerasuolo, A. Pollio, G. Pinto & M. DellaGreca, 2007. Allelopathy and competition between Chlorella vulgaris and Pseudokirchneriella subcapitata: Experiments and mathematical model. Ecology Modelling 208: 205–214.

    Article  Google Scholar 

  • Gebrehiwot, M., D. Kifle & L. Triest, 2017. Emergent Macrophytes Support Zooplankton in a Shallow Tropical Lake: A Basis for Wetland Conservation. Environmental Management 60: 1127–1138.

    Article  PubMed  Google Scholar 

  • Ghobrial, M. G., H. S. Nassr & A. W. Kamil, 2015. Bioactivity effect of two macrophyte extracts on growth performance of two bloom-forming cyanophytes. The Egyptian Journal Aquatic Research 41: 69–81.

    Article  Google Scholar 

  • Gross, E. M., S. Hilt, P. Lombardo & G. Mulderij, 2007. Searching for allelopathic effects of submerged macrophytes on phytoplankton—state of the art and open questions. Hydrobiologia 584: 77–88.

    Article  CAS  Google Scholar 

  • He, Y., Q. H. Zhou, B. Y. Liu, L. Cheng, Y. Tian, Y. Zhang & Z. B. Wu, 2016. Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system. Journal of Applied Phycology 28: 2805–2814.

    Article  CAS  Google Scholar 

  • Hillebrand, H., C. Durselen, D. Kírsctel, U. Polligher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

    Article  Google Scholar 

  • Hilt (nee Körner), S., 2006. Allelopathic inhibition of epiphytes by submerged macrophytes. AquaticBotanic 85 (3): 252–256

  • Hilt, S. & E. M. Gross, 2008. Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic and Applied Ecology 9: 422–432.

    Article  Google Scholar 

  • Holland, A. & S. Kinnear, 2013. Interpreting the possible ecological role (s) of cyanotoxins: compounds for competitive advantage and/or physiological aide? Mar Drugs 11: 239–2258.

    Article  Google Scholar 

  • Kaminski, A., B. Bober, E. Chrapusta & J. Bialczyk, 2014. Phytoremediation of anatoxin-a by aquatic macrophyte Lemna trisulca L. Chemosphere 112: 305–310.

    Article  CAS  PubMed  Google Scholar 

  • Kaminski, A., E. Chrapusta, B. Bober, M. Adamski, E. Latkowska & J. Bialczyk, 2015. Aquatic macrophyte Lemna trisulca (L.) as a natural factor for reducing anatoxin-a concentration in the aquatic environment and biomass of cyanobacterium Anabaena flos-aquae (Lyngb.) de Bréb. Algal Research 9: 212–217.

    Article  Google Scholar 

  • Kaplan, A., M. Harel, R. N. Kaplan-Levy, O. Hadas, A. Sukenik & E. Dittmann, 2012. The languages spoken in the water body (or the biological role of cyanobacterial toxins). Frontiers in Microbiology 3: 1–13.

    Article  Google Scholar 

  • Korner, S. & A. Nicklisch, 2002. Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes1. Jounal Phycology 38: 862–871.

    Article  Google Scholar 

  • Leão, P. N., M. T. S. D. Vasconcelos & V. M. Vasconcelos, 2009. Allelopathic activity of cyanobacteria on green microalgae at low cell densities. European Journal of Phycology 44: 347–355.

    Article  Google Scholar 

  • Li, Y. & D. Li, 2011. Competition between toxic Microcystis aeruginosa and nontoxic Microcystis wesenbergii with Anabaena PCC7120. Journal of Applied Phycology 24: 69–78.

    Article  CAS  Google Scholar 

  • Li, J., Y. Liu, P. Zhang, G. Zeng, X. Cai, S. Liu, Y. Yin, X. Hu, X. Hu & X. Tan, 2016. Growth inhibition and oxidative damage of Microcystis aeruginosa induced by crude extract of Sagittaria trifolia tubers. Journal of Environmental Sciences 43: 40–47.

    Article  Google Scholar 

  • Lürling, M., G. Van Geest & M. Scheffer, 2006. Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes Chara, Elodea and Myriophyllum. Hydrobiologia 556: 209–220.

    Article  Google Scholar 

  • Maredová, N., J. Altman & J. Kaštovský, 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of the Total Environment 792: 148413.

    Article  PubMed  Google Scholar 

  • Mohamed, Z. A., 2017. Macrophytes-cyanobacteria allelopathic interactions and their implications for water resources management—A review. Limnologica 63: 122–132.

    Article  CAS  Google Scholar 

  • Mohamed, Z. A. & Abdulrahman M. Al. S, 2010. Differential Responses of Epiphytic and Planktonic Toxic Cyanobacteria to Allelopathic Substances of the Submerged Macrophyte Stratiotes aloides. International Review of Hydrobiology 95(3): 224–234.

  • Nakai, S., Y. Inoue, M. Hosomi & A. Murakami, 1999. Growth inhibition of blue-green algae by allelopathic effects of macrophytes. Water Science & Technology 39: 47–53.

    Article  Google Scholar 

  • Nimptsch, J., C. Wiegand & S. Pflugmacher, 2008. Cyanobacterial Toxin Elimination via Bioaccumulation of MC-LR in Aquatic Macrophytes: An Application of the “Green Liver Concept.” Environmental Science & Technology 42: 8552–8557.

    Article  CAS  Google Scholar 

  • Pei, Y., L. Liu, S. Hilt, R. Xu, B. Wang, C. Li & X. Chang, 2018. Root exudated algicide of Eichhornia crassipes enhances allelopathic effects of cyanobacteria Microcystis aeruginosa on green algae. Hydrobiologia 823: 67–77.

    Article  Google Scholar 

  • Perreault, F., M. Seleme Matias, S. Pedroso Melegari, C. R. S. de Carvalho Pinto, E. Ekué Creppy, R. Popovic & W. Gerson Matias, 2011. Investigation of animal and algal bioassays for reliable saxitoxin ecotoxicity and cytotoxicity risk evaluation. Ecotoxicology and Environmental Safety 74: 1021–1026.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team., 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna,Austria. URL https://www.R-project.org/.

  • Romero-Oliva, C. S., V. Contardo-Jara & S. Pflugmacher, 2015. Antioxidative response of the three macrophytes Ceratophyllum demersum, Egeria densa, and Hydrilla verticillata to a time dependent exposure of cell-free crude extracts containing three microcystins from cyanobacterial blooms of Lake Amatitlan, Guatemala. Aquatic Toxicology 163: 130–139.

    Article  CAS  PubMed  Google Scholar 

  • Senavirathna, M. D. H. J., G. Muhetaer, K. S. Senarathna, K. S. S. Atapaththu & T. Fujino, 2021. Egeria densa Allelopathy on Microcystis aeruginosa Under Different Light Intensities and Preliminary Insight into Inter-Parameter Relationships. Water Air Soil Pollution 232: 135.

    Article  CAS  Google Scholar 

  • Sukenik, A., A. Quesada & N. Salmaso, 2015. Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodiversity and Conservation 24: 889–908.

    Article  Google Scholar 

  • Švanys, A., R. Paškauskas & S. Hilt, 2014. Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737: 57–66.

    Article  Google Scholar 

  • Tazart, Z., M. Douma, L. Tebaa & M. Loudiki, 2018. Use of macrophytes allelopathy in the biocontrol of harmful Microcystis aeruginosa blooms. Water Supply 19: 245–253.

    Article  Google Scholar 

  • Vanderstukken, M., N. Mazzeo, W. Van Colen, S. A. Declerck & K. Muylaert, 2011. Biological control of phytoplankton by the subtropical submerged macrophytes Egeria densa and Potamogeton illinoensis: a mesocosm study. Freshwater Biology 56: 1837–1849.

    Article  CAS  Google Scholar 

  • Wang, Z., J. Zhang, E. Li, L. Zhang, X. Wang & L. Song, 2017. Combined toxic effects and mechanisms of microsystin-LR and copper on Vallisneria Natans (Lour.) Hara seedlings. Journal of Hazardous Materials 328: 108–116.

    Article  CAS  PubMed  Google Scholar 

  • Wood, A. M., R. C. Everroad & L. M. Wingard, 2005. Measuring growth rates in microalgal cultures. In Andersen, R. A. (ed), Algal culturing techniques, Vol. 5. Academic Press, Singapore: 269–285.

    Google Scholar 

  • Wu, Z., P. Deng, X. Wu, S. Luo & Y. Gao, 2007. Allelopathic effects of the submerged macrophyte Potamogeton malaianus on Scenedesmus obliquus. Hydrobiologia 592: 465–474.

    Article  CAS  Google Scholar 

  • Wu, Z., J. Shi & S. Yang, 2013. The effect of pyrogallic acid on growth, oxidative stress, and gene expression in Cylindrospermopsis raciborskii (Cyanobacteria). Ecotoxicology 22: 271–278.

    Article  CAS  PubMed  Google Scholar 

  • Zehnsdorf, A., A. Hussner, F. Eismann, H. Rönicke & A. Melzer, 2015. Management options of invasive Elodea nuttallii and Elodea canadensis. Limnologica 51: 110–117.

    Article  Google Scholar 

  • Zhu, J., B. Liu, J. Wang, Y. Gao & Z. Wu, 2010. Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquatic Toxicology 98: 196–203.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the FAPESQ (Foundation for Research Support of the State of Paraíba) and CNPq (National Council for Scientific and Technological Development), (process 88887.142333 / 2017-00) for the financing of this study; the PPGCTA-UEPB (Environmental Engineering Post-Graduation Program of State University of Paraíba) and the Ecology Aquatic Laboratory team-UEPB for the support during the research time.

Funding

The funded was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant No. 88887.142333 / 2017–0).

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All authors contributed to the study conception. VVB, JdSS, and RDdSS contributed to data curation; VVB and RDdSS contributed to formal analysis; VVB and JdSS provided methodology; JEdLB and JdSS provided resources; JdSS and JEdLB performed supervision; VVB, RDdSS, and MAC contributed to writing of the original draft; VVB, JdSS, MAC, and JEdLB contributed to writing, reviewing, & editing of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Vanessa Virginia Barbosa.

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Barbosa, V.V., dos Santos Silva, R.D., dos Santos Severiano, J. et al. Can the presence of green microalgae reverse the allelopathic effects of the submerged macrophyte Egeria densa on the toxin-producing cyanobacterium Raphidiopsis raciborskii?. Hydrobiologia 849, 4391–4406 (2022). https://doi.org/10.1007/s10750-022-04997-4

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