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South American PSP toxin-producing Cylindrospermopsis raciborskii (Cyanobacteria) decreases clearance rates of cladocerans more than copepods

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Abstract

Toxic effects of freshwater cyanobacteria on mesozooplankton partially depend on the feeding strategies, generalist (cladocera) or selective filter-feeders (copepod) and on the type of toxin. Blooms of Cylindrospermopsis raciborskii (Nostocales) are increasingly more common in freshwaters. It can produce neurotoxins (paralytic shellfish poison, PSP), particularly in warm regions of the Americas. The knowledge about the effects of these neurotoxins on the clearance rate of zooplankton from warm regions still lags behind that of other world regions. We compared the toxin profile (using HPLC), morphology and growth rates of two PSP-producing C. raciborskii strains from South America. We evaluated the effect of these two strains on the clearance rate of two medium-sized grazers typical from subtropical and tropical environments, the copepod Notodiaptomus iheringi (~1.1 mm) and the cladoceran Daphnia pulex (~0.8 mm) in 2.5 h experiments. We found differences in the PSP profile, toxicity and morphology of the two C. raciborskii strains. Medium-sized predators were able to remove filaments of both strains in a similar amount despite their morphological and toxin differences. However, cladocera were significantly more affected than copepods in their clearance rates, suggesting differential consequences for their survival and success in warm freshwaters.

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References

  • Amaral, V., S. Bonilla & L. Aubriot, 2014. Growth optimization of the invasive cyanobacterium Cylindrospermopsis raciborskii in response to phosphate fluctuations. European Journal of Phycology 49: 134–141.

    Article  CAS  Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth.

    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 

  • Bonilla, S., L. Aubriot, M. C. S. Soares, M. González-Piana, A. Fabre, V. Huszar, M. Lürling, D. Antoniades, J. Padisák & C. Kruk, 2012. What drives the distribution of the bloom forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology 79: 594–607.

    Article  CAS  PubMed  Google Scholar 

  • Bouvy, M., M. Pagano & M. Troussellier, 2001. Effects of a cyanobacterial bloom (Cylindrospermopsis raciborskii) on bacteria and zooplankton communities in Ingazeira reservoir (northeast Brazil). Aquatic Microbial Ecology 25: 215–227.

    Article  Google Scholar 

  • Castro, D., D. Vera, N. Lagos, C. García & M. Vásquez, 2004. The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon 44: 483–489.

    Article  CAS  PubMed  Google Scholar 

  • Cestèle, S. & W. Catterall, 2000. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82: 883–892.

    Article  PubMed  Google Scholar 

  • Chorus, I. & J. Bartram, 1999. Toxic Cyanobacteria in Water: A guide to their public health consequences, monitoring and management. WHOE & FN Spon, London.

    Book  Google Scholar 

  • da Costa, S. M., S. da Ferrão-Filho & S. M. F. O. Azevedo, 2013. Effects of saxitoxin- and non-saxitoxin-producing strains of the cyanobacterium Cylindrospermopsis raciborskii on the fitness of temperate and tropical cladocerans. Harmful Algae 28: 55–63.

    Article  CAS  Google Scholar 

  • Deeds, J. R., J. H. Landsberg, S. M. Etheridge, G. C. Pitcher & S. W. Longan, 2008. Non-traditional vectors for paralytic shellfish poisoning. Marine Drugs 6: 308–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrão-Filho, A. S., M. C. S. Soares, V. Freitas de Magalhães & S. M. F. O. Azevedo, 2009. Biomonitoring of cyanotoxins in two tropical reservoirs by cladoceran toxicity bioassays. Ecotoxicology and Environmental Safety 72: 479–489.

    Article  CAS  Google Scholar 

  • Ferrão-Filho, A. S., M. C. S. Soares, V. Freitas de Magalhães & S. M. F. O. Azevedo, 2010. A rapid bioassay for detecting saxitoxins using a Daphnia acute toxicity test. Environmental Pollution 158: 2084–2093.

    Article  CAS  Google Scholar 

  • Ferrão-Filho, A. S., L. E. C. Galvão & V. Freitas de Magalhães, 2014. Differential susceptibility of cladoceran species to a saxitoxin-producer strain of Cylindrospermopsis raciborskii (cyanobacteria). Ecotoxicology and Environmental Contamination 9: 33–41.

    Article  Google Scholar 

  • Fulton, R. S., 1988. Grazing on filamentous algae by herbivorous zooplankton. Freshwater Biology 20: 263–271.

    Article  Google Scholar 

  • Ger, K. A., R. Panosso & M. Lürling, 2011. Consequences of acclimation to Microcystis on the selective feeding behavior of the calanoid copepod Eudiaptomus gracilis. Limnology and Oceanography 56: 2103–2114.

    Article  Google Scholar 

  • Ger, K. A., P. Urrutia-Cordero, P. C. Frost, L. Hansson, O. Sarnelle, A. E. Wilson & M. Lu, 2016. The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54: 128–144. doi:10.1016/j.hal.2015.12.005.

  • Gugger, M., R. Molica, B. Le Berre, P. Dufour, C. Bernard & J.-F. Humbert, 2005. Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents. Applied and Environmental Microbiology 71: 1097–1100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haande, S., T. Rohrlack, A. Ballot, K. Røberg, R. Skulberg, M. Beck & C. Wiedner, 2008. Genetic characterisation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) isolates from Africa and Europe. Harmful Algae 7: 692–701.

    Article  CAS  Google Scholar 

  • Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

    Article  Google Scholar 

  • Iglesias, C., N. Mazzeo, M. Meerhoff, G. Lacerot, J. M. Clemente, F. Scasso, C. Kruk, G. Goyenola, J. García-Alonso, S. L. Amsinck, J. C. Paggi, S. José de Paggi & E. Jeppesen, 2011. High predation is of key importance for dominance of smallbodied zooplankton in warm shallow lakes: evidence from lakes, fish exclosures and surface sediments. Hydrobiologia 667: 133–147.

    Article  Google Scholar 

  • Jeppesen, E., M. Meerhoff, B. A. Jacobsen, R. S. Hansen, M. Søndergaard, J. P. Jensen, T. L. Lauridsen, N. Mazzeo & W. C. Branco, 2007. Restoration of shallow lakes by nutrient control and biomanipulation – the successful strategy varies with lake size and climate. Hydrobiologia 581: 269–285.

    Article  CAS  Google Scholar 

  • Kâ, S., J. M. Mendoza-Vera, M. Bouvy, G. Champalbert, R. N’Gom-Kâ & M. Pagano, 2012. Can tropical freshwater zooplankton graze efficiently on cyanobacteria? Hydrobiologia 679: 119–138.

    Article  CAS  Google Scholar 

  • Kirk, K. L. & J. J. Gilbert, 1992. Variation in herbivore response to chemical defenses: zooplankton foraging on toxic cyanobacteria. Ecology 73: 2208–2217.

    Article  Google Scholar 

  • Koski, M., K. Schmidt, J. Engstrom-Ost, M. Viitasalo, S. Jonasdottir, S. Repka & K. Sivonen, 2002. Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena. Limnology and Oceanography 47: 878–885.

    Article  Google Scholar 

  • Lacerot, G., C. Kruk, M. Lürling & M. Scheffer, 2013. The role of subtropical zooplankton as grazers of phytoplankton under different predation levels. Freshwater Biology 58: 494–503.

    Article  Google Scholar 

  • Lagos, N., H. Onodera, P. A. Zagatto, D. Andrinolo, S. M. F. O. Azevedo & Y. Oshima, 1999. The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37: 1359–1373.

    Article  CAS  PubMed  Google Scholar 

  • Lukas, B., C. Hummert & Y. Oshima, 2004. Analytical methods for paralytic shellfish poisons. In Hallegraedd, G. M., D. M. Anderson & A. D. Cebella (eds), Manual on Harmful Marine Microalgae. UNESCO publishing, Paris: 191–209.

    Google Scholar 

  • Lürling, M. & A. Verschoor, 2003. FO-spectra of chlorophyll fluorescence for the determination of zooplankton grazing. Hydrobiologia 491: 145–157.

    Article  Google Scholar 

  • Lürling, M. & W. Beekman, 2006. Palmelloids formation in Chlamydomonas reinhardtii: defence against rotifer predators? Annales de Limnologie – International Journal of Limnology 42: 65–72.

    Article  Google Scholar 

  • Molica, R., H. Onodera, C. García, M. Rivas, D. Andrinolo, S. Nascimento, H. Meguro, Y. Oshima, S. Azevedo & N. Lagos, 2002. Toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycologia 41: 606–611.

    Article  Google Scholar 

  • Neilan, B. A., M. L. Saker, J. Fastner, A. Törökné & B. P. Burns, 2003. Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Molecular Ecology 12: 133–140.

    Article  CAS  PubMed  Google Scholar 

  • Neilan, B., L. Pearson, J. Muenchhoff, M. C. Moffitt & E. Dittmann, 2013. Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environmental Microbiology 15: 1239–1253.

    Article  CAS  PubMed  Google Scholar 

  • Oshima, Y., 1995. Post-column derivatization HPLC methods for paralytic shellfish poisons. In Hallegraedd, G. M., D. M. Anderson & A. D. Cebella (eds), Manual on Harmful Marine Microalgae. UNESCO publishing, Paris: 81–84.

    Google Scholar 

  • Padisák, J., 1997. Cylindrospermopsis raciborskii (Woloszyska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv Für Hydrobiologie Supplement 107: 563–593.

    Google Scholar 

  • Panosso, R. & M. Lürling, 2010. Daphnia magna feeding on Cylindrospermopsis raciborskii: the role of food composition, filament length and body size. Journal of Plankton Research 10: 1393–1404.

    Article  CAS  Google Scholar 

  • Panosso, R., B. Kozlowsky-Suzuki, S. M. F. O. Azevedo & E. Granéli, 2003. Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. Journal of Plankton Research 25: 1169–1175.

    Article  Google Scholar 

  • Piccini, C., L. Aubriot, A. Fabre, V. Amaral, M. González-Piana, A. Giani, C. C. Figueredo, L. Vidal, C. Kruk & S. Bonilla, 2011. Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10: 644–653.

    Article  Google Scholar 

  • Piccini, C., A. Fabre, G. Lacerot & S. Bonilla, 2015. Combining immunolabeling and catalyzed reporter deposition to detect intracellular saxitoxin in a cyanobacterium. Journal of Microbiological Methods 117: 18–21.

    Article  CAS  PubMed  Google Scholar 

  • Rangel, L. M., K. A. Ger, L. H. S. Silva, M. C. S. Soares, E. J. Faassen & M. Lürling, 2016. Toxicity overrides morphology on Cylindrospermopsis raciborskii grazing resistance to the calanoid copepod Eudiaptomus gracilis. Microbial Ecology. doi:10.1007/s00248-016-0734-8.

    PubMed  PubMed Central  Google Scholar 

  • Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Rocha, O. & A. Duncan, 1985. The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. Journal of Plankton Research 7: 279–294.

    Article  Google Scholar 

  • Sinha, R., L. Pearson, T. W. Davis, M. Burford, P. T. Orr & B. Neilan, 2012. Increased incidence of Cylindrospermopsis raciborskii in temperate zones – is climate change responsible? Water Research 46: 1408–1419.

    Article  CAS  PubMed  Google Scholar 

  • Sinha, R., L. Pearson, T. W. Davis, J. Muenchhoff, R. Pratama, A. Jex, M. Burford & B. A. Neilan, 2014. Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. Biomedical Central Genomics 15: 83.

    Google Scholar 

  • Soares, M. C. S., L. O. Vidal, F. Roland & V. L. M. Huszar, 2009. Cyanobacterial equilibrium phases in a small tropical impoundment. Journal of Plankton Research 31: 1331–1338.

    Article  Google Scholar 

  • Soares, M. C. S., V. L. M. Huszar, M. N. Miranda, M. M. Mello, F. Roland & M. Lürling, 2013. Cyanobacterial dominance in Brazil: distribution and environmental preferences. Hydrobiologia 717: 1–12.

    Article  CAS  Google Scholar 

  • Sommer, U. & H. Stibor, 2002. Copepoda–Cladocera–Tunicata: the role of three major mesozooplankton groups in pelagic food webs. Ecological Research 17: 161–174.

    Article  Google Scholar 

  • Soto-Liebe, K., A. Murillo, B. Krock, K. Stucken, J. J. Fuentes-Valdés, N. Trefault, A. Cembella & M. Vásquez, 2010. Reassessment of the toxin profile of Cylindrospermopsis raciborskii T3 and function of putative sulfotransferases in synthesis of sulfated and sulfonated PSP toxins. Toxicon 56: 1350–1361.

    Article  CAS  PubMed  Google Scholar 

  • Sukenik, A., O. Hadas, A. Kaplan & A. Quesada, 2012. Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes – Physiological, regional, and global driving forces. Frontiers in Microbiology 3: 86.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiese, M., P. M. D´Agostino, T. K. Mihali & M. C. Moffitt, 2010. Neurotoxic alkaloids: anaxitoxin and its analogues. Marine Drugs 8: 2185–2211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yilmaz, M. & E. J. Phlips, 2011. Toxicity and genetic diversity of Cylindrospermopsis raciborskii in Florida, USA. Lake and Reservoir Management 27: 235–244.

    Article  CAS  Google Scholar 

  • Yilmaz, M., E. J. Phlips, N. J. Szabo & S. Badylak, 2008. A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51: 130–139.

    Article  CAS  PubMed  Google Scholar 

  • Yunes, J. S., N. T. Cunha & L. P. Barros, 2003. Cyanobacterial neurotoxins from Southern Brazilian freshwaters. Comments on Toxicology 9: 103–115.

    Article  CAS  Google Scholar 

  • Zagatto, P. A., S. V. Buratini, M. A. Aragão & A. S. Ferrão-Filho, 2012. Neurotoxicity of two Cylindrospermopsis raciborskii (Cyanobacteria) strains to mice, Daphnia and fish. Environmental Toxicology and Chemistry 31: 857–862.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Iollanda Ivanov for her help during the copepod experiments, Ricardo Frederico Guedes de Souza for technical help with HPLC and Armando Vieira for kindly providing the strain of Chlamydomonas chlorastera used in this study. We thank Mathieu Cusson for his assistance with statistical analyses. This work was partially financed by PEDECIBA-Biología and CAP from Universidad de la República, and by the grant ANII-FCE6384.

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Authors and Affiliations

  1. Grupo de Ecología & Fisiología de Fitoplancton, Montevideo, Uruguay

    Amelia Fabre, Gissell Lacerot & Sylvia Bonilla

  2. Sección Limnología, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    Amelia Fabre & Sylvia Bonilla

  3. Ecología Funcional de Sistemas Acuáticos, Centro Universitario de la Región Este, Universidad de la República, Montevideo, Uruguay

    Gissell Lacerot

  4. Departamento de Engenharia Sanitária e Ambiental, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil

    Rafael Rodriguez de Paiva & M. Carolina S. Soares

  5. Instituto de Biofísica Carlos Chagas Filho, Laboratório de Ecofisiologia e Toxicologia de Cianobactéria, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Valéria Freitas de Magalhães

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  1. Amelia Fabre
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  2. Gissell Lacerot
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Correspondence to Amelia Fabre.

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Fabre, A., Lacerot, G., de Paiva, R.R. et al. South American PSP toxin-producing Cylindrospermopsis raciborskii (Cyanobacteria) decreases clearance rates of cladocerans more than copepods. Hydrobiologia 785, 61–69 (2017). https://doi.org/10.1007/s10750-016-2903-7

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