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Nutrient Enrichment Regulates the Growth and Physiological Responses of Saccharina japonica to Ocean Acidification

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Abstract

Environmental changes, such as ocean acidification and eutrophication, have created threats to kelp mariculture. In this study, the growth, photosynthesis, respiration and nutrient composition of Saccharina japonica were evaluated at different levels of pCO2 (400 and 800 μL L−1) and nutrients (nutrient-enriched and non-enriched seawater). Elevated pCO2 decreased the relative growth rate (RGR), net photosynthetic rate and contents of tissue carbon and tissue nitrogen under non-enriched nutrient conditions, but it had no significant effect on these parameters under nutrient-enriched conditions. The dark respiration rate was positively affected by elevated pCO2 regardless of the nutrient conditions. However, the C:N was unaffected by elevated pCO2 at both nutrient levels. These results implied that ocean acidification could reduce the production and nutrient contents in the tissues of S. japonica, which was associated with nutrient conditions.

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References

  • Agatsuma, Y., Endo, H., Yoshida, S., Ikemori, C., Takeuchi, Y., Fujishima, H., Nakajima, K., Sano, M., Kanezaki, N., Imai, H., Yamamoto, N., Kanahama, H., Matsubara, T., Takahashi, S., Isogai, T., and Taniguchi, K., 2014. Enhancement of Saccharina kelp production by nutrient supply in the Sea of Japan off southwestern Hokkaido, Japan. Journal of Applied Phycology, 26 (4): 1845–1852.

    Google Scholar 

  • Amthor, J. S., 1991. Respiration in a future, higher CO2 world. Plant Cell Environment, 14: 13–20.

    Google Scholar 

  • Boderskov, T., Schmedes, P. S., Bruhn, A., Rusmussen, M. B., Nielsen, M. M., and Pedersen, M. F., 2016. The effect of light and nutrient availability on growth, nitrogen, and pigment contents of Saccharina latissima (Phaeophyceae) grown in outdoor tanks, under natural variation of sunlight and temperature, during autumn and early winter in Denmark. Journal of Applied Phycology, 28 (2): 1153–1165.

    Google Scholar 

  • Celis-Plá, P. S. M., Martínez, B., Korbee, N., Hall-Spencer, J. M., and Figuero, F. L., 2017. Photoprotective responses in a brown macroalgae Cystoseira tamariscifolia to increases in CO2 and temperature. Marine Environmental Research, 130: 157–165.

    Google Scholar 

  • Chen, B., Lin, L., Ma, Z., Zhang, T., Chen, W., and Zou, D., 2019. Carbon and nitrogen accumulation and interspecific competition in two algae species, Pyropia haitanensis and Ulva lactuca, under ocean acidification conditions. Aquaculture International, 27: 721–733.

    Google Scholar 

  • Crawford, N. M., 1995. Nitrate: Nutrient and signal for plant growth. The Plant Cell, 7 (7): 859–868.

    Google Scholar 

  • Dawes, C. J., and Koch, E. W., 1990. Physiological responses of the red algae Gracilaria verrucosa and G. tikvahiae before and after nutrient enrichment. Bulletin of Materials Sciences, 46 (2): 335–344.

    Google Scholar 

  • Dickson, A. G., 1990. Standard potential of the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4- in synthetic seawater from 273.15 to 318.15 K. The Journal of Chemical Thermodynamics, 22 (2): 113–127.

    Google Scholar 

  • Endo, H., Okumura, Y., Sato, Y., and Agatsuma, Y., 2017. Interactive effects of nutrient availability, temperature, and irradiance on photosynthetic pigments and color of the brown alga Undaria pinnatifida. Journal of Applied Phycology, 29 (3): 1683–1693.

    Google Scholar 

  • Falkenberg, L. J., Russell, B. D., and Connell, S. D., 2013. Contrasting resource limitations of marine primary producers: Implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia, 172 (2): 575–583.

    Google Scholar 

  • Flynn, K. J., Blackford, J. C., Baird, M. E., Raven, J. A., Clark, D. R., Beardall, J., Brownlee, C., Fabian, H., and Wheeler, G. L., 2012. Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change, 2 (7): 510–513.

    Google Scholar 

  • Gao, G., Gao, Q., Bao, M., Xu, J., and Li, X., 2019. Nitrogen availability modulates the effects of ocean acidification on biomass yield and food quality of a marine crop, Pyropia yezoensis. Food Chemistry, 271: 623–629.

    Google Scholar 

  • Gao, K., and McKinley, K., 1994. Use of macroalgae for marine biomass production and CO2 remediation: A review. Journal of Appllied Phycology, 6: 45–60.

    Google Scholar 

  • Gao, K., Ji, Y., and Aruga, Y., 1999. Relationship of CO2 concentrations to photosynthesis of intertidal macroalgae during emersion. Hydrobiologia, 398: 355–359.

    Google Scholar 

  • Gao, X., Endo, H., Nagaki, M., and Agatsuma, Y., 2017. Interactive effects of nutrient availability and temperature on growth and survival of different size classes of Saccharina japonica (Laminariales, Phaeophyceae). Phycology, 56 (3): 253–260.

    Google Scholar 

  • García-Sânchez, M. J., Fernândez, J. A., and Niell, F. X., 1994. Effect of inorganic carbon supply on the photosyntetic physiology of Gracilaria tenuistipitata. Planta, 194 (1): 55–61.

    Google Scholar 

  • Geertz-Hansen, O., Sand-Jensen, K., Hansen, D. F., and Christiansen, A., 1993. Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary. Aquatic Botany, 46 (2): 101–109.

    Google Scholar 

  • Gordillo, F. J. L., Aguilera, J., Wiencke, C., and Jiménez, C., 2015. Ocean acidification modulates the response of two Arctic kelps to ultraviolet radiation. Journal of Plant Physiology, 173: 41–50.

    Google Scholar 

  • Gordon, T. O., and Carol, S. T., 2017. Divergent responses in growth and nutritional quality of coastal macroalgae to the combination of increased pCO2 and nutrients. Marine Environmental Research, 131: 69–79.

    Google Scholar 

  • Graham, M. H., 2004. Effects of local deforestation on the diversity and structure of Southern California giant kelp forest food webs. Ecosystems, 7 (4): 341–357.

    Google Scholar 

  • Gutow, L., Rahman, M. M., Bartl, K., Saborowski, R., Bartsch, I., and Wiencke, C., 2014. Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). Journal of Experimental of Marine Biology and Ecology, 453: 84–90.

    Google Scholar 

  • Huang, Y., Liu, X., Laws, E. A., Chen, B., Li, Y., Xie, Y., Wu, Y., Gao, K., and Huang, B., 2018. Effects of increasing atmospheric CO2 on the marine phytoplankton and bacterial metabolism during a bloom: A coastal mesocosm study. Science of the Total Environment, 633: 618–629.

    Google Scholar 

  • Hwang, E. U., Liu, F., Lee, K. H., Ha, D. S., and Park, C. S., 2018. Comparison of the cultivation performance between Korean (Sugwawon No. 301) and Chinese strains (Huangguan No. 1) of kelp Saccharina japonica in an aquaculture farm in Korea. Algae, 33 (1): 101–108.

    Google Scholar 

  • Iñiguez, C., Carmona, R., Lorenzo, M. R., Niell, F. X., Wiencke, C., and Gordillo, F. J. L., 2016. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta. Polar Biology, 39: 1979–1991.

    Google Scholar 

  • IPCC, 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker, T. F., et al., eds., Cambridge University Press, Cambridge, United Kingdom and New York, 1535pp.

  • IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Pachauri, R. K., and Meyer, L. A., eds., IPCC, Geneva, 151pp.

  • Israel, A., Katz, S., Dubinsky, Z., Merrill, J. E., and Friedlander, M., 1999. Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhorophyta). Journal of Applied Phycology, 11 (5): 447–453.

    Google Scholar 

  • Ji, Z., Zou, D., Gong, J., Liu, C., Ye, C., and Chen, Y., 2019. The different responses of growth and photosynthesis to NH4+ enrichments between Gracilariopsis lemaneiformis and its epiphytic alga Ulva lactuca grown at elevated atmospheric CO2. Marine Pollution Bulletin, 144: 173–180.

    Google Scholar 

  • Johnson, M. D., Comeau, S., Lantz, C. A., and Smith, J. E., 2017. Complex and interactive effects of ocean acidification and temperature on epilithic and endolithic coral-reef turf algal assemblages. Coral Reefs, 36: 1059–1070.

    Google Scholar 

  • Kang, J. W., and Chung, I. K., 2017. The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. Journal of Applied Phycology, 29: 2675–2683.

    Google Scholar 

  • Kang, J. W., and Chung, I. K., 2018. The interactive effects of elevated CO2 and ammonium enrichment on the physiological performances of Saccharina japonica (Laminariales, Phaeophyta). Ocean Science Journal, 53 (3): 487–497.

    Google Scholar 

  • Kim, J. H., Kang, E. J., Edwards, M. S., Lee, K., Jeong, H. J., and Kim, K. Y., 2016. Species-specific responses of temperate macroalgae with different photosynthetic strategies to ocean acidification: A mesocosm study. Algae, 31 (3): 243–256.

    Google Scholar 

  • Lewis, E., and Wallace, D., 1998. Program Developed for CO2 System Calculations. Carbon Dioxide Information Analysis Center. Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee.

    Google Scholar 

  • Liu, F., Wang, X., Liu, J., Fu, W., Duan, D., and Yang, Y., 2009. Genetic mapping of the Laminaria japonica (Laminariales, Phaeophyta) using amplified fragment length polymorphism markers. Journal of Phycology, 45 (5): 1228–1233.

    Google Scholar 

  • Ménesguen, A., Desmit, X., Dulière, V., Lacroix, G., Thouvenin, B., Thieu, V., and Dussauze, M., 2018. How to avoid eutrophication in coastal seas? A new approach to derive river-specific combined nitrate and phosphate maximum concentrations. Science of the Total Environment, 628: 400–414.

    Google Scholar 

  • Mercado, J., Javier, F., Gordillo, L., Niell, F. X., and Figueroa, F., 1999. Effects of different levels of CO2 on photosynthsis and cell components of the red alga Porphyra leucosticta. Journal of Applied Phycology, 11 (5): 455–461.

    Google Scholar 

  • Mizuta, H., Narumi, H., and Yamamoto, H., 2001. Effects of nitrate and phosphate on the growth and maturation of gametophytes of Laminaria religiosa Miyabe (Phaeophyceae). Suisanzoshoku, 49: 175–180 (in Japanese with English abstract).

    Google Scholar 

  • Oh, J. C., Yu, O. H., and Choi, H. G., 2015. Interactive effects of increased temperature and pCO2 concentration on the growth of a brown algae Ecklonia cava in the sporophyte and gametophyte stages. Ocean and Polar Research, 37 (3): 201–209.

    Google Scholar 

  • Olischlaeger, M., Bartsch, I., Gutow, L., and Wiencke, C., 2012. Effects of ocean acidification on different life-cycle stages of the kelp Laminaria hyperborea (Phaeophyceae). Botanica Marina, 55 (5): 511–525.

    Google Scholar 

  • Qu, L., Xu, J., Sun, J., Li, X., and Gao, K., 2017. Diurnal pH fluctuations of seawater influence the responses of an economic red macroalga Gracilaria lemaneiformis to future CO2-induced seawater acidification. Aquaculture, 473: 383–388.

    Google Scholar 

  • Raven, J. A., Giordano, M., Beardall, J., and Maberly, S. C., 2012. Algal evolution in relation to atmospheric CO2: Carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philosophical Transactions of the Royal Society, 367: 493–507.

    Google Scholar 

  • Rost, B., Riebesell, U., Burkhardt, S., and Siiltemeyer, D., 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography, 48: 55–67.

    Google Scholar 

  • Roy, R. N., Roy, L. N., Vogel, K. M., Porter-Moore, C., Pearson, T., Good, C. E., Millero, F. J., and Campbell, D. M., 1993. The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperature 0 to 45?. Marine Chemistry, 44 (2-4): 249–267.

    Google Scholar 

  • Russell, B. D., Thompson, J. A. I., Falkenberg, L. J., and Connell, S. D., 2009. Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Global Change Biology, 15: 2153–2162.

    Google Scholar 

  • Schmid, R., Mills, J., and Dring, M., 1996. Influence of carbon supply on the stimulation of light-saturated photosynthesis by blue light in Laminaria saccharina: Implications for mechanism of carbon acquisition in higher brown algae. Plant Cell Environment, 19 (4): 383–391.

    Google Scholar 

  • Selivanova, O. N., Zhigadlova, G. G., and Hansen, G. I., 2007. Revision of the systematics of algae in the order Laminariales (Phaeophyta) from the Far-Eastern Seas of Russia on the basis of molecular-phylogenetic data. Russian Journal of Marine Biology, 33 (5): 278–289.

    Google Scholar 

  • Smith, S. V., Swaney, D. P., Talaue-Mcmanus, L., Bartley, J. D., Sandhei, P. T., McLaughlin, C. J., Dupra, V. C., Crossland, C. J., Buddemeier, R. W., Maxwell, B. A., and Wulff, F., 2003. Humans, hydrology, and the distribution of inorganic nutrient loading to the ocean. Bioscience, 53 (3): 235–245.

    Google Scholar 

  • Spijkerman, E., 2011. The expression of a carbon concentrating mechanism in Chlamydomonas acidophila under variable phosphorus, iron, and CO2 concentrations. Photosynthesis Research, 109 (1-3): 179–189.

    Google Scholar 

  • Suárez-Álvarez, S., Gómez-Pinchetti, J. L., and García-Reina, G., 2012. Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). Journal of Applied Phycology, 24: 815–823.

    Google Scholar 

  • Swanson, A. K., and Fox, C. H., 2007. Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs. Global Change Biology, 13 (8): 1696–1709.

    Google Scholar 

  • Tatewaki, M., 1966. Formation of a crustose sporophyte with unilocular sporangia in Scitosiphon lomentaria. Phycologia, 6: 62–66.

    Google Scholar 

  • Wu, H., Ding, G., and Xu, Z., 2015. Effects of salt stress on growth and photosynthesis of Pyropia haitanensis (Rhodophyta) cultured under different nitrogen conditions. Oceanologia et Limnologia Sinica, 46: 1210–1217 (in Chinese with English abstract).

    Google Scholar 

  • Wu, Y., Gao, K., and Riebesell, U., 2010. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences, 7: 2915–2923.

    Google Scholar 

  • Xu, D., Brennan, G., Xu, L., Zhang, X. W., Fan, X., Han, W., Mock, T., McMinn, A., Hutchins, D. A., and Ye, N., 2019. Ocean acidification increases iodine accumulation in kelp-based coastal food webs. Global Change Biology, 25: 629–639.

    Google Scholar 

  • Xu, D., Wang, D., Li, B., Fan, X., Zhang, X., Ye, N., Wang, Y., Mou, S., and Zhuang, Z., 2015. Effects of CO2 and seawater acidification on the early stages of Saccharina japonica development. Environmental Science & Technology, 49 (6): 3548–3556.

    Google Scholar 

  • Xu, J., and Gao, K., 2012. Future CO2-induced ocean acidification mediate the physiological performance of a green tide alga. Plant Physiology, 160 (4): 1762–1769.

    Google Scholar 

  • Xu, Z., Gao, G., and Xu, J., 2017. Physiological response of a golden tide alga (Sargassum muticum) to the interaction of ocean acidification and phosphorus enrichment. Biogeosciences, 14 (3): 671–681.

    Google Scholar 

  • Yang, G., and Gao, K., 2012. Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity. Marine Environmental Research, 79: 142–151.

    Google Scholar 

  • Zou, D., 2005. Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture, 250: 726–735.

    Google Scholar 

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Acknowledgements

We would like to thank the reviewers for their helpful comments that improve the manuscript. This research was supported by Ocean University of China in 2018 and the Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (No. 2019JZZY020708).

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Correspondence to Yan Liu or Qingli Gong.

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Chu, Y., Liu, Y., Li, J. et al. Nutrient Enrichment Regulates the Growth and Physiological Responses of Saccharina japonica to Ocean Acidification. J. Ocean Univ. China 19, 895–901 (2020). https://doi.org/10.1007/s11802-020-4359-7

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  • DOI: https://doi.org/10.1007/s11802-020-4359-7

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