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Effects of light intensity and nutrients (N and P) on growth, toxin concentration, heterocyte formation and akinete germination of Nodularia spumigena (Cyanobacteria)

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Abstract

Harmful effects of the toxic cyanobacterium Nodularia spumigena were observed in experimental marine shrimp production ponds in Brazil. Strains of this cyanobacterial species were isolated and cultured, and in the present study, we evaluated the influence of light intensity and the concentration of dissolved inorganic nitrate and phosphate on the growth, toxin concentration, heterocyte formation and akinete germination of N. spumigena. A factorial experiment (3 × 3) was performed to test three light intensities and nutrient concentrations with a reduced nitrate concentration, a reduced phosphate concentration and a nutrient-replete f/2 medium. The influence of light intensity on growth and akinete formation was varied: the highest cell density and chlorophyll a were recorded at the lowest light intensity, while the high light treatment stimulated akinete formation. The availability of phosphate was the main factor favouring the growth of N. spumigena and the formation and germination of akinetes, while the concentration of nodularin per cell was highest under phosphate deficiency. This information is useful in the management of aquaculture ponds and other brackish and marine environments where the goal is to reduce N. spumigena blooms.

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References

  • Baker, P. D. & D. Bellifemine, 2000. Environmental influences on akinete germination of Anabaena circinalis and implications for management of cyanobacterial blooms. Hydrobiologia 427: 65–73.

    Article  Google Scholar 

  • Björkman, O. & B. Demming-Adams, 1994. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In Schulze, E.-D. & M. M. Caldwell (eds), Ecophysiology of Photosynthesia. Springer, Berlin: 17–47.

    Google Scholar 

  • Blackburn, S., M. A. McCausland, C. J. S. Bolch, S. J. Newman & G. J. Jonas, 1996. Effect of salinity on growth and toxin production in cultures of the bloom-forming cyanobacterium Nodularia spumigena from Australian waters. Phycologia 35: 511–522.

    Article  Google Scholar 

  • Boopathi, T. & J. Ki, 2014. Impact of environmental factors on the regulation of cyanotoxin production. Toxins 6: 1951–1978.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Briand, J. F., C. Leboulanger, J. F. Humbert, C. Bernard & P. Dufour, 2004. Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology 40: 231–238.

    Article  Google Scholar 

  • Costa, C. M., G. K. Fóes, C. Odebrecht, L. Poersh & W. Wasielesky, 2013. Impacto da cianobactéria Nodularia spumigena em cultivo de camarões marinhos em sistema de bioflocos. Reunião Latino Americana Sobre Algas Nocivas.

  • Duarte, C. M., S. Agustí & N. S. R. Agawin, 2000. Response of a Mediterranean phytoplankton community to increased nutriente inputs: a mesocosm experiment. Marine Ecology Progress Series 195: 61–70.

    Article  Google Scholar 

  • Dyble, J., P. A. Tester & R. W. Litaker, 2006. Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. African Journal of Marine Science 28: 308–312.

    Article  Google Scholar 

  • Fay, P., J. A. Lynn & S. C. Majer, 1984. Akinete development in the planktonic blue-green alga Anabaena circinalis. British Phycological Journal 19: 163–173.

    Article  Google Scholar 

  • Guillard, R. R. L., 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & M. H. Chanley (eds), Culture of Marine Invertebrate Animals. Plenum, New York: 29–60.

    Chapter  Google Scholar 

  • Hense, I. & A. Beckmann, 2006. Towards a model of cyanobacteria life cycle-effects of growing and resting stages on bloom formation of N2-fixing species. Ecological Modelling 195: 205–218.

    Article  Google Scholar 

  • Hobson, P. & H. Fallowfield, 2001. Effect of salinity on photosynthetic activity of Nodularia spumigena. Journal of Applied Phycology 13: 493–499.

    Article  Google Scholar 

  • Hobson, P. & H. J. Fallowfield, 2003. Effect of irradiance, temperature and salinity on growth and toxin production by Nodularia spumigena. Hydrobiologia 493: 7–15.

    Article  CAS  Google Scholar 

  • Huber, A. L., 1985. Factors affecting the germination of akinetes of Nodularia spumigena (Cyanobacteriaceae). Applied Environmental Microbiology 49: 73–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibelings, B. W., 1996. Changes in photosynthesis in response to combined irradiance and temperature stress in cyanobacterial surface waterblooms. Journal of Phycology 32: 549–557.

    Article  Google Scholar 

  • Jodlowska, S. & A. Latala, 2010. Photoacclimation strategies in the toxic cyanobacterium Nodularia spumigena (Nostocales, Cyanobacteria). Phycologia 49: 203–211.

    Article  CAS  Google Scholar 

  • Komárek, J., 2013. Cyanoprokaryota -3. Teil/Part 3: Heterocytous genera. In: Büdel, B., Gärtner, G., Krienitz, L., Schagerl, M. (eds) Süßwasserflora von Mitteleuropa Freshwater flora of Central Europe. Springer/Spektrum, Heidelberg.

  • Kononen, K., 1992. Dynamics of the toxic cyanobacterial blooms in the Baltic Sea. Finnish Marine Research 261: 3–36.

    Google Scholar 

  • Kononen, K., J. Kuparinen & K. Mäkelä, 1996. Initiation of cyanobacterial blooms in a frontal region at the entrance to the Gulf of Finland, Baltic Sea. Limnology and. Oceanography 41: 98–112.

    Article  CAS  Google Scholar 

  • Latasa, M. & E. Berdalet, 1994. Effect of nitrogen or phosphorus starvation on pigment composition of cultured Heterocapsa sp. Journal of Plankton Research 16: 83–94.

    Article  Google Scholar 

  • Lehtimäki, J., K. Sivonem, R. Luukkainem & S. I. Niemelä, 1994. The effects of incubation time, temperature, light, salinity, and phosphorus on growth and hepatotoxin production by Nodularia strain. Archiv für Hydrobiologie 130: 269–282.

    Article  Google Scholar 

  • Lehtimäki, J., P. Moisander, K. Sivonen & K. Kononen, 1997. Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Applied Environmental Microbiology 63: 1647–1656.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, R., M. Watanabe & M. M. Watanabe, 1997. Akinete formation in planktonic Anabaena spp. (cyanobacteria) by treatment with low temperature. Journal of Phycology 33: 576–584.

    Article  Google Scholar 

  • Loreto, C., N. Rosales, J. Bermúdez & E. Morales, 2003. Producción de pigmentos y proteínas de la cianobacteria Anabaena PCC 7120 em relación a la concentración de nitrógeno e irradiancia. Gayna Botánica 60: 83–90.

    Google Scholar 

  • Ma, J., N. Lu, W. Qin, R. Xu, Y. Wang & X. Chen, 2006. Differential responses of eight cyanobacterial and green algal species, to carbamate insecticides. Ecotoxicology and Environmental Safety 63: 268–274.

    Article  CAS  PubMed  Google Scholar 

  • Mackinney, G., 1941. Absorption of light by chlorophyll solutions. Journal of Biological Chemistry 140: 315–322.

    Article  CAS  Google Scholar 

  • Mazur-Marzec, H., L. Źeglińska & M. Pliński, 2005. The effect of salinity on the growth, toxin production, and morphology of Nodularia spumigena isolated from the Gulf of Gdańsk, southern Baltic Sea. Journal of Applied Phycology 17: 171–179.

    Article  CAS  Google Scholar 

  • Mazur-Marzec, H., M. Bertos-Fortis, A. Toruńska-Sitarz, A. Fidor & C. Legrand, 2016. Chemical and genetic diversity of Nodularia spumigena from the Baltic Sea. Marine Drugs 14: 1–14.

    Article  CAS  Google Scholar 

  • Misha, S. K., A. Shrivastav, R. R. Maurya, S. K. Patidar, S. Haldar & S. Mishra, 2012. Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp. isolated from Gujarat coast, India. Protein Expression and Purification 81: 5–10.

    Article  CAS  Google Scholar 

  • Mohlin, M. & A. Wulff, 2009. Interaction effects of ambient UV radiation and nutrient limitation on the toxic cyanobacterium. Microbial Ecology 57: 675–686.

    Article  PubMed  Google Scholar 

  • Mohlin, M., M. Y. Roleda, B. Pattanaik, S. J. Tenne & A. Wulff, 2012. Interspecific resource competition-combined effects of radiation and nutrient limitation on two diazotrophic filamentous cyanobacteria. Microbial Ecology 63: 736–750.

    Article  PubMed  Google Scholar 

  • Moisander, P. H. & H. W. Paerl, 2000. Growth, primary productivity, and nitrogen fixation potential of Nodularia spp. (Cyanophyceae) in water from a subtropical estuary in the United States. Journal of Phycology 36: 645–658.

    Article  CAS  PubMed  Google Scholar 

  • Moisander, P. H., E. McClinton III & H. W. Paerl, 2002. Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic cyanobacteria. Microbial Ecology 43: 432–442.

    Article  CAS  PubMed  Google Scholar 

  • Moore, D., M. O’Donohue, G. Shaw & C. Critchley, 2003. Potential triggers for akinete differentiation in an Australian strain of the cyanobacterium Cylindrospermopsis raciborskii (AWT 205/1). Hydrobiologia 506: 175–180.

    Article  Google Scholar 

  • Moore, D., M. O’Donohue, C. Garnett & G. S. Critchley, 2005. Factors affecting akinete differentiation in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria). Freshwater Biology 50: 345–352.

    Article  Google Scholar 

  • Muramatsu, M. & Y. Hihara, 2012. Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses. Journal of Plant Research 125: 11–39.

    Article  CAS  PubMed  Google Scholar 

  • Musial, A. & M. Pliński, 2003. Influence of salinity on the growth of Nodularia spumigena Mertens. Oceanological and Hydrobiological Studies 32: 45–52.

    Google Scholar 

  • Myers, J. H., J. Beardall, G. Allinson, S. Salzman & L. Gunthorpe, 2010. Environmental influences on akinete germination and development in Nodularia spumigena (Cyanobacteriaceae), isolated from the Gippsland Lakes, Victoria, Australia. Hydrobiologia 649: 239–247.

    Article  CAS  Google Scholar 

  • Myers, J. H., J. Beardall, G. Allinson, S. Salzman, S. Robertson & L. Gunthorpe, 2011. Potential triggers of akinete differentiation in Nodularia spumigena (Cyanobacteriaceae) isolated from Australia. Hydrobiologia 671: 165–180.

    Article  CAS  Google Scholar 

  • Niemi, A., 1979. Blue-green algal blooms and N:P ratio in the Baltic Sea. Acta Botanica Fennica. 110: 57–61.

    CAS  Google Scholar 

  • Odebrecht, C., 1998. Radiação fotossinteticamente ativa em Rio Grande. Documentos Técnicos 8. Rio Grande, Brasil.

  • Pacheco, L. A., N. Kunrath, C. M. Costa, L. D. F. Costa, G. K. Foes, W. Wasielesky & J. S. Yunes, 2016. Identification of the toxic pentapeptide nodularin in a cyanobacterial bloom in a shrimp farm in south american atlantic coast. Pharmaceutica Analytica Acta 7: 5.

    Google Scholar 

  • Padisak, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) 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 

  • Paes, C. R. P. S., G. R. Faria, N. A. B. Tinoco, D. J. F. A. Castro, E. Barbarino & S. O. Lourenço, 2016. Growth, nutrient uptake and chemical composition of Chlorella sp. and Nannochloropsis oculata under nitrogen starvation. Latin American Journal of Aquatic Research 44: 275–292.

    Article  Google Scholar 

  • Pattanaik, B., A. Wulff, M. Y. Roleda, K. Garde & M. Mohlin, 2010. Production of the cyanotoxin nodularin – a multifactorial approach. Harmful Algae 10: 30–38.

    Article  CAS  Google Scholar 

  • Pliński, M. & T. Jóźwiak, 1999. Temperature and N:P ratio as factors causing blooms of blue-green algae in the Gulf of Gdánsk. Oceanologia 41: 73–80.

    Google Scholar 

  • Popin, R. V., E. Delbaje, V. A. C. Abreu, J. Rigonato, F. A. Dörr, E. Pinto, K. Sivonen & M. F. Fiore, 2020. Genomic and metabolomic analyses of natural products in Nodularia spumigena isolated from a srimp culture pond. Toxins 12: 141.

    Article  CAS  PubMed Central  Google Scholar 

  • Rinehart, K. L., K. Harada, M. Namikoshi, C. Chen, C. A. Harvis, M. H. G. Munro, J. W. Blunt, P. E. Mulligan, V. R. Beasley, A. M. Dahlem & W. W. Carmichael, 1988. Nodularin, microcystin, and the configuration of adda. Journal of the American Chemical Society 110: 8557–8558.

    Article  CAS  Google Scholar 

  • Roleda, M. Y., M. Mohlin, B. Pattanaik & A. Wulff, 2008. Photosynthetic response of Nodularia spumigena to UV and photosynthetically active radiation depends on nutrient (N and P) availability. FEMS Microbiology Ecology 66: 230–242.

    Article  CAS  PubMed  Google Scholar 

  • Ruivo, M., A. Amorium & P. Cartaxana, 2011. Effects of growth phase and irradiance on phytoplankton pigments ratios: implications for chemotaxonomy in coastal waters. Journal of Plankton Research 33: 1012–1022.

    Article  CAS  Google Scholar 

  • Silveira, S. B. & C. Odebrecht, 2019. Effects of salinity and temperature on the growth, toxin production, and akinete germination of the cyanobacterium Nodularia spumigena. Frontiers in Marine Science 6: 339.

    Article  Google Scholar 

  • Silveira, S. B., W. Wasielesky, A. P. D. Andreote, M. F. Fiore & C. Odebrecht, 2017. Morphology phylogeny, growth rate and nodularin production of Nodularia spumigena from Brazil. Marine Biology Research 13: 1095–1107.

    Article  Google Scholar 

  • Sivonen, K. & G. Jones, 1999. Cyanobacterial toxins. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. E&FN Spon, London: 55–124.

    Google Scholar 

  • Smith, V. H., 2007. Using primary productivity as an index of coastal eutrophication: the units of measurement matter. Journal of plankton research 29: 1–6.

    Article  CAS  Google Scholar 

  • Stal, L. J. & A. E. Walsby, 2000. Photosynthesis and nitrogen fixation in a cyanobacterial bloom in the Baltic Sea. European Journal of Phycology 35: 97–109.

    Article  Google Scholar 

  • Stal, L. J., M. Staal & M. Willbrandt, 1999. Nutrient control of cyanobacterial bloom in the Baltic Sea. Aquatic Microbial Ecology 18: 165–173.

    Article  Google Scholar 

  • Stal, M., S. L. Hekkert, P. Herman & L. J. Stal, 2002. Comparison of models describing light dependence of N2 fixation in heterocystous cyanobacteria. Applied and Environmental Microbiology 68: 4679–4683.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stal, L. J., P. Albertano, B. Bergman, K. von Bröckel, J. R. Gallon, P. K. Hayes, K. Sivonen & A. E. Walsby, 2003. BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea—responses to a changing environment. Continental Shelf Research 23: 1695–1714.

    Article  Google Scholar 

  • Strickland, J. D. H. & T. R. Parsons, 1972. A Practical Handbook of Seawater Analysis, 2nd ed. Fisheries Research Board of Canada, Bulletin 167, Ottawa.

    Google Scholar 

  • Sukenik, A., J. Beardall & O. Hadas, 2007. Photosynthetic characterization of developing and mature akinetes of Aphanizomenon ovalisporum (Cyanoprokaryota). Journal of Phycology 43: 780–788.

    Article  CAS  Google Scholar 

  • Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.

    Article  Google Scholar 

  • Thompson, P. A., I. Jameson & S. I. Blackburn, 2009. The influence of light quality on akinete formation and germination in the toxic cyanobacterium Anabaena circinalis. Harmful Algae 8: 504–512.

    Article  CAS  Google Scholar 

  • Van den Hoek, C., D. G. Mann & H. M. Jahns, 1995. Algae: An Introduction to Phycology. Cambridge University Press, Austrália: 627.

    Google Scholar 

  • Van Dok, W. & B. T. Hart, 1996. Akinete differentiation in Anabaena circinalis (Cyanophyta). Journal of Phycology 32: 557–565.

    Article  Google Scholar 

  • Van Dok, W. & B. T. Hart, 1997. Akinete germination in Anabaena circinalis (Cyanophyta). Journal of Phycology 33: 12–17.

    Article  Google Scholar 

  • Vijaya, V. & N. Anand, 2009. Blue light enhance the pigment synthesis in cyanobacterium Anabaena ambigua Rao (Nostocales). Journal of Agricultural and Biological Science 4: 36–43.

    Google Scholar 

  • Wallström, K., S. Johansson & U. Larsson, 1992. Effect of nutrient enrichment on planktonic blue-green algae in the Baltic Sea. Acta Phytogeographica Suecica 78: 25–31.

    Google Scholar 

  • Wulff, A., M. Mohlin & K. Sundbäck, 2007. Intraspecific variation in the response of the cyanobacterium Nodularia spumigena to moderate UV-B radiation. Harmful Algae 6: 388–399.

    Article  CAS  Google Scholar 

  • Yunes, J. S., S. De La Rocha, D. Giroldo, S. B. Silveira, R. Comin, M. S. Bicho, S. S. Melcher, C. L. Sant’anna & A. A. H. Vieira, 2009. Release of carbohydrates and proteins by a subtropical strain of Raphidiopsis brookii (Cyanobacteria) able to produce saxitoxin at three nitrate concentrations. Journal of Phycology 45: 585–591.

    Article  CAS  PubMed  Google Scholar 

  • Zar, J. H., 2010. Biostatistical Analysis, 5th ed. Pearson, New Jersey.

    Google Scholar 

  • Zhu, C. J. & Y. K. Lee, 1997. Determination of biomass dry weight of marine microalgae. Journal of Applied Phycology 9: 189–194.

    Article  Google Scholar 

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Acknowledgments

We would like to thank Dr.Wilson Wasielesky for providing the experimental shrimp ponds of the Marine Station of Aquaculture (EMA), Federal University of Rio Grande-FURG. We are also grateful for the constructive criticism provided by the reviewers that helped improving the manuscript. Financial support was provided through the Brazilian Long-term Ecological Research of the Ministry of Sciences/National Research Council (CNPQ, Proc. 403805/2012-0; FAPERGS Proc. 3122-2551/12-7) to C.O. and the Ministry of Education (CAPES) graduate grant to S. B. S.

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Silveira, S.B., Odebrecht, C. Effects of light intensity and nutrients (N and P) on growth, toxin concentration, heterocyte formation and akinete germination of Nodularia spumigena (Cyanobacteria). Hydrobiologia 848, 4387–4400 (2021). https://doi.org/10.1007/s10750-021-04649-z

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