Abstract
Pyropia is a genus of algae used in sushi. Nitrate (NO3−) is essential for its growth. Excess NO3− is flushed into seawater, as a result of anthropogenic activities, increasing the potential for higher than normal concentrations which could be harmful to both algae and humans. This study aims to evaluate the effect of NO3− on the morphology, ultrastructure, spore viability, autofluorescence of chloroplasts, and formation of cell wall, during germination of the red seaweed Pyropia acanthophora var. brasiliensis. To accomplish this, carpospores were cultivated at 24°C, 40 μmol photons m−2 s−1 with photoperiod of 12 h and exposed to 0, 25, 50, and 100 mM of NO3− for 2 days. Samples were cultured for another 5 days to measure the length of the germ tube. Concentrations of NO3− did not significantly influence the development, morphology, viability, or ultrastructure of the spores in the first 2 days. The absence of this nutrient did delay the ultrastructural development of the carpospore, decreasing autofluorescence of the chloroplast and delaying the formation of the cell wall and pyrenoid. Over the seven-day experimental period, higher concentrations of NO3− increased the size of the germ tube, indicating that this extra concentration boosted the development of P. acanthophora.
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References
Abe, K., A. Imamaki & M. Hirano, 2002. Removal of nitrate, nitrite, ammonium and phosphate ions from water by the aerial microalga Trentepohlia aurea. Journal of Applied Phycology 1: 129–134.
Baird, C. & M. Cann, 2011. Química Ambiental, 4a ed. Bookman, Porto Alegre.
Bao Do, C. & F. Cormier, 1991. Effects of low nitrate and high sugar concentrations on anthocyanin content and composition of grape (Vitis vinifera L.) cell suspension. Plant Cell Reports 9: 500–504.
Barufi, J. B., N. Korbee, M. C. Oliveira & F. L. Figueroa, 2011. Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilaria tenuistipitata (Rhodophyta) cultured under UV radiation. Journal of Applied Phycology 23: 457–466.
Blouin, N. A., J. A. Brodie, A. C. Grossman, P. Xu & S. H. Brawley, 2011. Porphyra: A marine crop shaped by stress. Trends in Plant Science 16(1): 29–37.
Bouzon, Z. L., L. C. Ouriques & E. C. De Oliveira, 2005. Ultrastructure of tetraspore germination in the agar-producing seaweed Gelidium floridanum (Gelidiales, Rhodophyta). Phycologia 44: 409–415.
Bouzon, Z. L., L. C. Ouriques & E. C. Oliveira, 2006. Spore adhesion and cell wall formation in Gelidium floridanum (Rhodophyta, Gelidiales). Journal of Applied Phycology 18: 287–294.
Camargo, J. A. & Á. Alonso, 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: A global assessment. Environment International 32: 831–849.
Chaloub, R. M., N. M. S. Motta, S. P. de Araujo, P. F. de Aguiar & A. F. da Silva, 2015. Combined effects of irradiance, temperature and nitrate concentration on phycoerythrin content in the microalga Rhodomonas sp. (Cryptophyceae). Algal Research Elsevier B.V. 8: 89–94.
Chen, J., F. Wu, W. Wang, C. Zheng, G. Lin, X. Dong, J. He, Z. Pei & H. Zheng, 2011. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. Journal of Experimental Botany 62: 4481–4493.
Corey, P., J. K. Kim, J. Duston, D. J. Garbary & B. Prithiviraj, 2013. Bioremediation potential of Palmaria palmata and Chondrus crispus (Basin Head): effect of nitrate and ammonium ratio as nitrogen source on nutrient removal. Journal of Applied Phycology 25: 1349–1358.
Do, C. B. & F. Cormier, 1991. Effects of low nitrate and high sugar concentrations on anthocyanin content and composition of grape (Vitis vinifera L.) cell suspension. Plant Cell Reproduction 9: 500–504.
Edwards, P., 1972. Cultured red alga to measure pollution. Marine Pollution Bulletin 3: 184–188.
Gahan, P. B., 1984. Plant histochemistry and cytochemistry. Academic Press, Cambridge.
Gauchazh, 2019. Florianópolis tem 20 pontos impróprios para banho; veja a lista. https://gauchazh.clicrbs.com.br/ambiente/noticia/2019/01/florianopolis-tem-20-pontos-improprios-para-banho-veja-a-lista-cjqjfocil0pkb01rxmzl3vjoq.html.
Glazer, A. N., 1994. Phycobiliproteins – a family of valuable, widely used fluorophores. Journal of Applied Phycology 6: 105–112.
Gordon-Mills, E. M. & E. L. McCandless, 1975. Carrageenans in the cell walls of Chondrus crispus Stack. (Rhodophyceae, Gigartinales) I. Localization with fluorescent antibody. Phycologia 14: 275–281.
Jeanfils, J., M. F. Canisius & N. Burlion, 1993. Effect of high nitrate concentrations on growth and nitrate uptake by free-living and immobilized Chlorella vulgaris cells. Journal of Applied Phycology 5: 369–374.
Kim, G. H. & L. Fritz, 1993. Gamete recognition during fertilization in a red alga, Antithamnion nipponicum. Protoplasma 174: 69–73.
Kshirsagar, A. D., 2013. Bioremediation of wastewater by using microalgae: An experimental study. International Journal of Life Sciences Biotechnology and Pharma Research 2: 339–346.
Li, Y., M. Horsman, B. Wang, N. Wu & C. Q. Lan, 2008. Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Applied Microbiology and Biotechnology 81: 629–636.
Martins, A. P., 2007. Efeitos da disponibilidade do nitrato no metabolismo do nitrogênio em variantes pigmentares de Hypnea musciformis (Wulfen in Jacqu.) J.V. Lamour. (Gigartinales, Rhodophyta). Dissertation of Botany Institute.
McCully, K. S. & B. D. Ragsdale, 1970. Production of Arteriosclerosis by Homocysteinemia. The American Journal of Pathology 61: 1–7.
Milstein, D., A. S. Medeiros, E. C. Oliveira & M. C. Oliveira, 2015. Native or introduced? A re-evaluation of Pyropia species (Bangiales, Rhodophyta) from Brazil based on molecular analyses. European Journal of Phycology 50(1): 37–45.
Miranda, R. D. S., R. O. Mesquita, N. S. Freitas, J. T. Prisco & E. Gomes-Filho, 2014. Nitrate: Ammonium nutrition alleviates detrimental effects of salinity by enhancing photosystem II efficiency in sorghum plants. Revista Brasileira de Engenharia Agrícola e Ambiental 18: 8–12.
Nunes, B. G., 2010. Monitoramento do ambiente do cultivo experimental da alga Kappaphycus alvarezii na Praia de Sambaqui, Florianópolis/SC.
Pereira, D. T., B. Pereira, A. Fonseca, F. Ramlov, M. Maraschin, F. Álvarez-Gómez, F. L. Figueroa, É. C. Schmidt, Z. L. Bouzon & C. Simioni, 2019. Effects of ultraviolet radiation (UV ‐A + UV ‐B) on the antioxidant metabolism of the red macroalga species Acanthophora spicifera (Rhodophyta, Ceramiales) from different salinity and nutrient conditions. Photochemistry and Photobiology XX: 1–11.
Pires, C. M., 2014. Análise do potencial de fertilização da macroalga Kappaphycus alvarezii com efluentes oriundos da carcinicultura de Litopenaeus vannamei em sistema de bioflocos. Trabalho de Conclusão de Curso da Universidade Federal de Santa Catarina.
Pueschel, C. M., 1979. Ultrastructure of tetrasporogenesis in Palmaria Palmata (Rhodophyta). Journal of Phycology 15: 409–424.
Reynolds, E. S., 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17: 208–212.
Ribeiro, A. L. N., K. E. Tesima, J. M. Souza & N. S. Yokoya, 2013. Effects of nitrogen and phosphorus availabilities on growth, pigment, and protein contents in Hypnea cervicornis J. Agardh (Gigartinales, Rhodophyta). J. Journal of Applied Phycology 25(4): 1151–1157.
Ribeiro, A. L. N., V. G. Chiozzini, E. S. Braga & N. S. Yokoya, 2017. Physiological responses and biofilter potential of Hypnea aspera (Rhodophyta, Gigartinales) cultivated in different availabilities of nitrate, ammonium, and phosphate. Journal of Applied Phycology 29(2): 683–694.
Santos, F. W. M., 2009. Período de permanência de cordas do mexilhão Perna perna (L., 1758) em cultivo. Trabalho de Conclusão de Curso da Universidade Federal de Santa Catarina.
Schmidt, É. C., L. A. Scariot, T. Rover & Z. L. Bouzon, 2009. Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40: 860–869.
Schweikert, K., J. E. S. Sutherland, C. L. Hurd & D. J. Burritt, 2011. UV-B radiation induces changes in polyamine metabolism in the red seaweed Porphyra cinnamomea. Plant Growth Regulation 65: 389–399.
Sharma, G. K. & S. A. Khan, 2013. Bioremediation of sewage wastewater using selective algae for manure production. International Journal of Environmental Engineering Management 4: 573–580.
Simioni, C., L. Hayashi & M. C. Oliveira, 2019. Seaweed resources of Brazil: what has changed in 20 years? Botanica Marina 62(5): 433–441.
Townsend, A. R., R. W. Howarth, F. A. Bazzaz, M. S. Booth, C. C. Cleveland, S. K. Collinge, A. P. Dobson, P. R. Epstein, E. A. Holland, D. R. Keeney, M. A. Mallin, C. A. Rogers, P. Wayne & A. H. Wolfe, 2003. Human health effects changing nigrogen cycle. Frontiers in Ecology and the Environment 1: 240–246.
Vesilind, P. A. & S. M. Morgan, 2013. Introdução à engenharia ambiental. Cengage Learning, São Paulo.
Wu, H., J. K. Kim, Y. Huo, J. Zhang & P. He, 2017. Nutrient removal ability of seaweeds on Pyropia yezoensis aquaculture rafts in China’s radial sandbanks. Aquatic Botany 137: 72–79.
Zhang, Q., N. Li, G. Zhou, X. Lu, Z. Xu & Z. Li, 2003. In vivo antioxidant activity of polysaccharide fraction from Porphyra haitanesis (Rhodophyta) in aging mice. Pharmacological Research 48: 151–155.
Zheng, Y. & K. Gao, 2009. Impacts of solar uv radiation on the photosynthesis, growth, and uv-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations. Journal of Phycology 45: 314–323.
Zhou, C., X. Yu, Y. Zhang, R. He & H. Ma, 2012. Ultrasonic degradation, purification and analysis of structure and antioxidant activity of polysaccharide from Porphyra yezoensis Udea. Carbohydrate Polymers Elsevier Ltd. 87: 2046–2051.
Zitta, C. S., T. Rover, L. Hayashi & Z. L. Bouzon, 2013. Callus ontogeny of the Kappaphycus alvarezii (Rhodophyta, Gigartinales) brown tetrasporophyte strain. Journal of Applied Phycology 25: 615–629.
Acknowledgements
The authors acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for the financial support to Zenilda Laurita Bouzon (process 449712/2014-1). This study is part of the Ph.D. thesis of the first author.
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Pereira, D.T., Ouriques, L.C., Bouzon, Z.L. et al. Effects of high nitrate concentrations on the germination of carpospores of the red seaweed Pyropia acanthophora var. brasiliensis (Rhodophyta, Bangiales). Hydrobiologia 847, 217–228 (2020). https://doi.org/10.1007/s10750-019-04083-2
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DOI: https://doi.org/10.1007/s10750-019-04083-2