Skip to main content
Log in

Effects of high nitrate concentrations on the germination of carpospores of the red seaweed Pyropia acanthophora var. brasiliensis (Rhodophyta, Bangiales)

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

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.

    Article  Google Scholar 

  • Baird, C. & M. Cann, 2011. Química Ambiental, 4a ed. Bookman, Porto Alegre.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Edwards, P., 1972. Cultured red alga to measure pollution. Marine Pollution Bulletin 3: 184–188.

    Article  CAS  Google Scholar 

  • Gahan, P. B., 1984. Plant histochemistry and cytochemistry. Academic Press, Cambridge.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kim, G. H. & L. Fritz, 1993. Gamete recognition during fertilization in a red alga, Antithamnion nipponicum. Protoplasma 174: 69–73.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Simioni, C., L. Hayashi & M. C. Oliveira, 2019. Seaweed resources of Brazil: what has changed in 20 years? Botanica Marina 62(5): 433–441.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Vesilind, P. A. & S. M. Morgan, 2013. Introdução à engenharia ambiental. Cengage Learning, São Paulo.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Débora Tomazi Pereira.

Additional information

Handling editor: Iacopo Bertocci

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04083-2

Keywords

Navigation