Advertisement

Journal of Ocean University of China

, Volume 18, Issue 1, pp 239–252 | Cite as

Influence of N, P, Fe Nutrients Availability on Nitrogen Metabolism- Relevant Genes Expression in Skeletonema marinoi

  • Xiaoli Jing
  • Tiezhu MiEmail author
  • Yu Zhen
  • Hualong Wang
  • Zhigang Yu
Article

Abstract

Nitrogen (N), Phosphorus (P), and Iron (Fe) are essential elements for cellular structure and metabolism. In addition to dissolved inorganic nitrogen (DIN), phytoplankton is able to utilize dissolved organic nitrogen (DON). There is general consensus that both bacteria and higher plants nitrogen metabolism is affected by phosphate availability; this was also found to be true in coccolithophorid. Iron affects the structure and function of ecosystems through its effects on nitrogen metabolism. However, it is unclear how these nutrients affect Skeletonema marinoi’s nitrogen metabolism. Here, using RT-qPCR, we investigate effects of N, P, and Fe on S. marinoi’s nitrogen metabolism and nitrate reductase activity. These results illuminate that in S. marinoi, various nutrients have direct regulation on these genes expression at the molecular level. The varying degree of responses for these genes expression with differing N sources may act to increase the efficiency of nutrient capture when nitrate is limited. Suitable gene expression occurs at a N/P ratio of 16, which represents the atomic N/P ratio of phytoplankton cells and N/P concentrations in ocean; thus, nitrogen metabolism gene expression should be regulated by the existing N/P ratios in the phytoplankton’s internal and external environment. Fe concentration has a direct and significant effect on nitrogen metabolism by regulating gene expression and nitrate reductase activity. Gene expression profiles identified in S. marinoi provide a foundation for understanding molecular mechanisms behind diatom nitrogen metabolism with changing N, P, and Fe nutrients allowing a basic understanding of how diatom growth is affected by nutrient utilization.

Key words

Skeletonema marinoi nitrogen metabolism relative gene expression RT-qPCR 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 41521064), the Scientific and Technological Innovation Project of the Qingdao National Laboratory for Marine Science and Technology (No. 2016ASKJ02) and the Public Science and Technology Research Funds Projects of Ocean (No. 201205031). We wish to thank Miss Brittany Sprecher from University of Connecticut for her help with English.

References

  1. Alipanah, L., Rohloff, J., Einge, P., Bones, A. M., and Brembu, T., 2015. Whole–cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum. Journnal of Experimental Botany, 66 (20): 6281–6296.CrossRefGoogle Scholar
  2. Allen, A. E., Ward, B. B., and Song, B., 2005. Characterization of diatom (Bacillariophyceae) nitrate reductase genes and their determination in marine phytoplankton communities. Journal of Phycology, 41: 95–104.CrossRefGoogle Scholar
  3. Allen, A. E., LaRoche, J., Maheswari, U., Lommer, M., Schauer, N., Lopez, P. J., and Bowler, C., 2008. Whole–cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proceedings of the National Academy of Sciences USA, 105 (30): 10438–10443.CrossRefGoogle Scholar
  4. Allen, A. E., and Dupont, C. L., 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature, 473: 203–207.CrossRefGoogle Scholar
  5. Antia, N. J., Berland, B. R., Bonin, D. J., and Maestrini, S. Y., 1975. Comparative evalution of certain organic and inorganic sources of nitrogen for phototrophic growth of marine microalgae. Marine Biological Association UK, 55: 519–539.CrossRefGoogle Scholar
  6. Antia, N. J., Harrison, P. J., and Oliveira, L., 1991. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia, 30: 1–89.CrossRefGoogle Scholar
  7. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., and Wilkerson, D., 2004. The genome of the diatom Thalassiosira pseudonana ecology, evolution and metabolism. Science, 306: 79–86.CrossRefGoogle Scholar
  8. Baker, K. M., Gobler, C. J., and Collier, J. L., 2009. Urease gene sequences from algae and heterotrophic bacteria in axenic and nonaxenic phytoplankton cultures. Journal of Phycology, 45: 625–634.CrossRefGoogle Scholar
  9. Banse, K., 1991. Rates of phytoplankton cell division in the field and in iron enrichment experiments. Limnology and Oceanography, 36 (8): 1886–1898.CrossRefGoogle Scholar
  10. Beman, J. M., Arrigo, K. R., and Matson, P. A., 2005. Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature, 434: 211–214.CrossRefGoogle Scholar
  11. Berg, G. M., Shrager, J., Glockner, G., Arrigo, K. R., and Grossman, A. R., 2008. Understanding nitrogen limitation in Aureococcus anophagefferens (Pelagophyceae) through cDNA and qRT–PCR analysis. Journal of Phycology, 44: 1235–1249.CrossRefGoogle Scholar
  12. Berges, J. A., and Harrison, P. J., 1995. Nitrate reductase–activity quantitatively predicts the rate of nitrate incorporation under steady–state light limitation: A revised assay and characteration of the enzyme in 3 species of marine–phytoplankton. Limnology and Oceanography, 40: 82–93.CrossRefGoogle Scholar
  13. Berges, J. A., 1997. Algal nitrate reductase. Europe Journal of Phycology, 32: 3–8.CrossRefGoogle Scholar
  14. Bowler, C., Allen, A. E., Badger, J. H., Grimwood, J., Jabbari, K., Kuo, A., and Grigoriev, I. V., 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456: 239–244.CrossRefGoogle Scholar
  15. Bowler, C., Vardi, A., and Allen, A. E., 2010. Oceanographic and biogeochemical insights from diatom genomes. Annual Review of Marine Science, 2: 333–365.CrossRefGoogle Scholar
  16. Brand, L. E., Sunda, W. G., and Guillard, R. L., 1983. Limitation of marine primary production rates by zinc, manganese, and iron. Limnology and Oceanography, 28: 1182–1198.CrossRefGoogle Scholar
  17. Brown, C. M., Macdonald–Brown, D., and Meers, J. L., 1974. Physiological aspects of microbial inorganic nitrogen metabolism. In Rose, A. H., and Tempest, D. W., eds., Advances in Microbial Physiology v.2 Academic, 1–52.CrossRefGoogle Scholar
  18. Capone, D. G., and Hutchins, D. A., 2013. Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nature Geoscience, 6: 711–717.CrossRefGoogle Scholar
  19. Carpenter, E. J., Remsen, C. C., and Schroeder, B. W., 1972a. Comparison of laboratory and in situ measurements of urea decomposition by a marine diatom. Journal of Experimental Marine Biology and Ecology, 8: 259–264.CrossRefGoogle Scholar
  20. Carpenter, E. J., Remsen, C. C., and Watson, S. W., 1972b. Utilization of urea by some marine phytoplankters. Limnology and Oceanography, 17: 265–269.CrossRefGoogle Scholar
  21. Chandrasekaran, R., Barra, L., Carillo, S., Caruso, T., Corsaro, L., Dal Piaz, F., and Brunet, C., 2014. Light modulation of biomass and macromolecular composition of the diatom Skeletonema marinoi. Journal of Biotechnology, 192: 114–122.CrossRefGoogle Scholar
  22. Cheng, C. L., Dewdney, J., Kleinhofs, A., and Goodman, H. M., 1986. Cloning and nitrate induction of nitrate reductase mRNA. Proceedings of the National Academy of Sciences USA. 83: 6825–6826.CrossRefGoogle Scholar
  23. Clayton, J. R., and Ahmed, S. I., 1986. Detection of glutamate synthase (GOGAT) activity in phytoplankton: Evaluation of cofactors and assay optimization. Marine Ecoloy Progress Series, 32: 115–122.CrossRefGoogle Scholar
  24. Dagenais–Bellefeuille, S., and Morse, D., 2013. Putting the N in dinoflagellates. Frontier Microbiology, 4: 369.Google Scholar
  25. Dham, V. V., Wafar, M. V. M., and Heredia, A. M., 2005. Nitrogen uptake by size–fractionated phytoplankton in mangrove water. Aquatic Microbial Ecology, 41: 281–291.CrossRefGoogle Scholar
  26. Dong, H. P., Huang, K. X., Wang, H. L., Lu, S. H., Cen, J. Y., and Dong, Y. L., 2014. Understanding strategy of nitrate and urea assimilation in a Chinese strain of Aureococcus anophagefferens through RNA–seq analysis. PLoS One, 9 (10): e111069.CrossRefGoogle Scholar
  27. Dortch, Q., Ahmed, S. I., and Packard, T., 1979. Nitrate reductase and glutamate dehydrogenase activities in Skeletonema costatum as measures of nitrogen assimilation rates. Journal of Plankton Research, 1: 169–186.CrossRefGoogle Scholar
  28. Dyhrman, S., and Palenik, B., 2003. Characterization of ectoenzyme activity and phosphate–regulated proteins in the coccolithophorid Emiliania huxleyi. Journal of Plankton Research, 25 (10): 1215–1225.CrossRefGoogle Scholar
  29. Estrada, M., and Blasco, D., 1979. 2 phases of the phytoplankton community in the Baja California upwelling. Limnology and Oceanography, 24: 1065–1080.CrossRefGoogle Scholar
  30. Fernandez, E., Galvan, A., and Quesada, A., 1998. Nitrogen assimilation and its regulation. Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, 7: 637–674.CrossRefGoogle Scholar
  31. Galangau, F., Daniel–Vedel, F., Moureaux, T., Dorbe, M. F., Leydecker, M. T., and Caboche, M., 1988. Expression of leaf nitrate reductase genes from tomato and tobacco in relation to light–dark regimes and nitrate supply. Plant Physiology, 88: 383–388.CrossRefGoogle Scholar
  32. Gao, Y., Smith, G. J., and Alberte, R. S., 1993. Nitrate reductase from the marine diatom Skeletonema costatum: Biochemical and immunological characterization. Plant Physiology, 103: 1437–1445.CrossRefGoogle Scholar
  33. Gonzalez–Ballester, D., De Montaigu, A., Higuera, J. J., Galvan, A., and Fernandez, E., 2005. Functional genomics of the regulation of the nitrate assimilation pathway in Chlamydomonas. Plant Physiology, 137: 522–533.CrossRefGoogle Scholar
  34. Graziano, M., and Lamattina, L., 2005. Nitric oxide and iron in plants: An emerging and converging story. Trends Plant Science, 10: 4–8.CrossRefGoogle Scholar
  35. Gruber, N., 2008. The Marine Nitrogen Cycle: Overview and Challenges in Nitrogen in the Marine Environment. 2nd ed. Academic Press, San Diego, 1–50.CrossRefGoogle Scholar
  36. Guillard, R. R. L., 1963. Organic sources of nitrogen for marine centric diatoms. Marine Microbiology, 93–104.Google Scholar
  37. He, S. Y., Yu, Z. G., and Mi, T. Z., 2009. Relationship between proliferating cell nuclear antigen gene expression amount and growth rate of Skeletonema costatum. Acta Hydrobiologica Sinica, 33 (1): 103–112 (in Chinese with English abstract).CrossRefGoogle Scholar
  38. Hockin, N. L., Mock, T., Mulholland, F., Kopriva, S., and Malin, G., 2012. The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiology, 158: 299–312.CrossRefGoogle Scholar
  39. Huber, J. L., Redinbaugh, M. G., Huber, S. C., and Campbell, W. H., 1994. Regulation of maize leaf nitrate reductase activity involves both gene expression and protein phosphorylation. Plant Physiology, 106: 1667–1674.CrossRefGoogle Scholar
  40. Iyer, V. R., Eisen, M. B., Ross, D. T., Schuler, G., Moore, T., Lee, J. C. F., and Brown, P. O., 1999. The transcriptional program in the response of human fibroblasts to serum. Science, 283: 83–87.CrossRefGoogle Scholar
  41. Jing, X. L., Mi, T. Z., Zhen, Y., Fu, B. Z., Li, C. F., and Yu, Z. G., 2016. Description of nitrogen metabolism pathway based on Skeletonema marinoi transcriptome. Marine Environmental Science, 35 (5): 703–711 (in Chinese with English abstract).Google Scholar
  42. Karl, D. M., 2000. Phosphorus, the staff of life. Nature, 406: 31–32.CrossRefGoogle Scholar
  43. Kubista, M., Andrade, J. M., Bengtsson, M., Forootan, A., Jona´k, J., Lind, K., and Zoric, N., 2006. The real–time polymerase chain reaction. Molecular Aspects of Medicine, 27: 95–125.CrossRefGoogle Scholar
  44. Kudela, R. M., and Dugdale, R. C., 2000. Nutrient regulation of phytoplankton productivity in Monterey Bay, California. Deep Sea Research II Topical Studies in Oceanography, 47: 1023–1053.CrossRefGoogle Scholar
  45. Lauritano, C., Borra, M., Carotenuto, Y., Biffali, E., Miralto, A., Procaccini, G., and Ianora, A., 2011a. First molecular evidence of diatom effects in the copepod Calanus helgolandicus. Journal of Experimental Marine Biology and Ecology, 404: 79–86.CrossRefGoogle Scholar
  46. Lauritano, C., Borra, M., Carotenuto, Y., Biffali, E., Miralto, A., Procaccini, G., and Ianora, A., 2011b. Molecolar evidence of the toxic effects of diatom diets on gene expression patterns in copepods. PLoS One, 6: e26850.Google Scholar
  47. Lauritano, C., Carotenuto, Y., Vitiello, V., Buttino, I., Romano, G., Hwang, J. S., Ianora A., 2015. Effects of the oxylipinproducing diatom Skeletonema marinoi on gene expression levels in the calanoid copepod Calanus sinicus. Marine Genomics, S1874–7787(15)00008–2.Google Scholar
  48. Lee, B., Yu, H., Jahoor, F., O’Brien, W., Beaudet, A. L., and Reeds, P., 2000. In vivo urea cycle flux distinguishes and correlates with phenotypic severity in disorders of the urea cycle. Proceedings of the National Academy of Sciences USA, 97: 8021–8026.CrossRefGoogle Scholar
  49. Li, M. Z., Li, L., Shi, X. G., Lin, L. X., and Lin, S. J., 2015. Effects of phosphorus deficiency and adenosine 5 ‘–triphosphate (ATP) on growth and cell cycle of the dinoflagellate Prorocentrum donghaiense. Harmful Algae, 47: 35–41.CrossRefGoogle Scholar
  50. Liaw, S. H., Jun, G., and Eisenberg, D., 1994. Interactions of nucleotides with fully unadenylylated glutamine synthetase from Salmonella typhimurium. Biochemistry, 33 (37): 11184.CrossRefGoogle Scholar
  51. Lin, S. J., Litaker, R. W., and Sunda, W. G., 2016. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. Journal of Phycology, 52: 10–36.CrossRefGoogle Scholar
  52. Liu, J. Q., Samac, D. A., Bucciarelli, B., Allan, D. L., Vance1, C. P., 2005. Signaling of phosphorus deficiency–induced gene expression in white lupin requires sugar and phloem transport. The Plant Journal, 41: 257–26.CrossRefGoogle Scholar
  53. Livak, K. J., and Schmittgen, T. D., 2001; Analysis of relative gene expression data using real time quantitative PCR and the 2–??CT Method. Methods, 25: 402–408.CrossRefGoogle Scholar
  54. Mann, K. H., 1993. Physical oceanography, food chains, and fish stocks: A review. ICES Journal of Marine Science, 50: 105–119.CrossRefGoogle Scholar
  55. Mathew, T., 1981. Nitrate reduction in Chlorococcales. Hydrobiologia, 79: 3–14.CrossRefGoogle Scholar
  56. McCarthy, J. J., and Eppley, R. W., 1972. A comparison of chemical, isotropic and enzymatic methods for measuring nitrogen assimilation of marine phytoplankton. Limnology and Oceanography, 17: 371–382.CrossRefGoogle Scholar
  57. Milligan, A. J., and Harrison, P. J., 2000. Effects of non–steadystate iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). Journal of Phycology, 36: 78–86.CrossRefGoogle Scholar
  58. Mobley, H. L. T., and Hausinger, R. P., 1989. Microbial ureases: Significance, regulation, and molecular characterization. Microbiological Reviews, 53: 85–108.Google Scholar
  59. Moore, J. K., Doney, S. C., Glover, D. M., and Fung, I. Y., 2002. Iron cycling and nutrient–limitation patterns in surface waters of the world ocean. Deep–Sea Research II, 49: 463–507.CrossRefGoogle Scholar
  60. Moore, C. M., Mills, M. M., Arrigo, K. R., Berman–Frank, I., Bopp, L., Boyd, P. W., and Ulloa, O., 2013. Processes and patterns of oceanic nutrient limitation. Nature Geoscience, DOI: 10.1038/NGEO1765.Google Scholar
  61. Morel, A., and Bricaud, A., 1986. Inherent optical properties of algal cells including picoplankton: Theoretical and experimental results. Canadian Journal of Fisheries and Aquatic Science, 214: 512–559.Google Scholar
  62. Morel, F. M. M., Hudson, R. J. M., and Price, N. M., 1991. Limitation of productivity by trace metals in the sea. Limnology and Oceanography, 36 (8): 1742–1755.CrossRefGoogle Scholar
  63. Morel, F. M. M., and Price, N. M., 2003. The biogeochemical cycles of trace metals in the oceans. Science, 300: 944–947.CrossRefGoogle Scholar
  64. Nalewajko, C. L., and Lean, D. R. S., 1980. The physiological ecology of phytoplankton. In: Phosphorus. Morris, I., ed., Black well Scientific, Oxford, 235–258.Google Scholar
  65. Orefice, I., Lauritano, C., Procaccini, G., Romano, G., and Ianora, A., 2015. Insights in possible cell–death markers in the diatom Skeletonema marinoi in response to senescence and silica starvation. Marine Genomics, 24: 81–88.CrossRefGoogle Scholar
  66. Orefice, I., Chandrasekaran, R., Smerilli, A., Corato, F., Carillo, S., Caruso, T., and Brunet, C., 2016. Light–induced changes in the photosynthetic physiology and biochemistry in the diatom Skeletonema marinoi. Algal Research, 17: 1–13.CrossRefGoogle Scholar
  67. Smerilli, A., Orifice, I., Corato, F., Ruban, A., and Brunet, C., 2017. Photoprotective and antioxidant responses to light spectrum and intensity variations in the coastal diatom Skeletonema marinoi. Environmental Microbiology, 19 (2): 611–627.CrossRefGoogle Scholar
  68. Paytan, A., and McLaughlin, K., 2007. The oceanic phosphorus cycle. Chemistry Reviews, 107: 563–76.CrossRefGoogle Scholar
  69. Rasmussen, R., 2001. Quantification on the lightcycler. In: Rapid Cycle Real–time PCR. Methods and Application. Meuer, S., et al., eds., Springer Press, Heidelberg, 21–34.CrossRefGoogle Scholar
  70. Raven, J. A., 1988. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytologist, 109: 279–287.CrossRefGoogle Scholar
  71. Redfield, A. C., 1958. The biological control of chemical factors in the environment. American Scientis, 46: 205–221.Google Scholar
  72. Rhee, G. Y., 1974. Phosphate uptake under nitrate limitation by Scenedesmus sp. Journal of Phycology, 10: 470–475.Google Scholar
  73. Rhee, G. Y., 1978. Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnology and Oceanography, 23: 10–25.CrossRefGoogle Scholar
  74. Ribalet, F., Wichard, T., Pohnert, G., Ianora, A., Miralto, A., and Casotti, R., 2007. Age and nutrient limitation enhance polyunsaturated aldehyde production in marine diatoms. Phytochemistry, 68: 2059–2067.CrossRefGoogle Scholar
  75. Rodriguez–Garcia, A., Sola–Landa, A., Apel, K., Santos–Beneit, F., and Martin, J. F., 2009. Phosphate control over nitrogen metabolism in Streptomyces coelicolor: Direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Research, 37 (10): 3230–3242.CrossRefGoogle Scholar
  76. Ryther, J., and Dunstan, W. M., 1971. Nitrogen, phosphorus and entrophication in the coastal marine environment. Science, 171: 1008–1013.CrossRefGoogle Scholar
  77. Sarno, D., Kooistra, W. H. C. F., Medlin, L. K., Percopo, I., and Zingone, A., 2005. Diversity in the genus Skeletonema (Bacillariophyceae). II An assessment of S. costatum–like species with the description of four new species. Journal of Phycology, 41: 151–176.Google Scholar
  78. Scheible, W. R., Gonzalez–Fontes, A., Lauerer, M., Muller–Rober, B., Caboche, M., and Stitt, M., 1997a. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell, 9: 783–98.CrossRefGoogle Scholar
  79. Scheible, W. R., Lauerer, M., Schulz, E. D., Caboche, M., and Stitt, M., 1997b. Accumulation of nitrate in the shoot acts as a signal to regulate shoot–root allocation in tobacco. Plant Journal, 11: 671–91.CrossRefGoogle Scholar
  80. Seethalakshmi, S., and Rao, N. A., 1979. Regulation of the activity of mung bean (Phaseolus aureus) glutamine synthetase by amino acids and nucleotides. Archives of Biochemistry and Biophysics, 196 (2): 588–97.CrossRefGoogle Scholar
  81. Shen, H., Hong, J. C., Zhang, K. F., Wang, G. L., and Lv, S. H., 1995. Studies on the effects of Fe and Mn in the Skeletonema costatum red tide. Journal of Jinan University (Natural Science), 16 (1): 131–149 (in Chinese with English abstract).Google Scholar
  82. Solomon, C. M., Collier, J. L., Berg, G. M., and Glibert, P. M., 2010. Role of urea in microbial metabolism in aquatic systems: A biochemical and molecular review. Aquatic Microbial Ecology, 59: 67–88.CrossRefGoogle Scholar
  83. Sunda, W. G., 1989. Trace mental interactions with marine phytoplankton. Biological Oceanography, 6: 411–442.Google Scholar
  84. Takabayashi, M., Wilkerson, F. P., and Robertson, D., 2005. Response of glutamine synthetase gene transcription and enzyme activity to external nitrogen sources in the diatom Skeletonema costatum (Bacillariophyceae). Journal of Phycology, 41: 84–94.CrossRefGoogle Scholar
  85. Uitz, J., Claustre, H., Gentili, B., and Stramski, D., 2010. Phytoplankton class–specifi primary production in the world’s oceans: Seasonal and inter annual variability from satellite observations. Global Biogeochemical Cycles, 24: GB3016.Google Scholar
  86. Wang, H. L., Mi, T. Z., Zhen, Y., Jing, X. L., Liu, Q., and Yu, Z. G., 2017. Metacaspases and programmed cell death in Skeletonema marinoi in response to silicate limitation. Journal of Plankton Research, 39 (4): 729–743.CrossRefGoogle Scholar
  87. Wagner, D., Wiemann, P., Huß, K., Brandt, U., Fleißner, A., and Tudzynski, B., 2013. A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi. PLoS One, 8 (11): e80740.CrossRefGoogle Scholar
  88. Wheeler, P. A., North, B. B., and Stephens, G. C., 1974. Amino acid uptake by marine phytoplankters. Limnology and Oceanography, MARC11V19(2).Google Scholar
  89. Yamamoto, T., and Tarutani, K., 1996. Growth and phosphate uptake kinetics of Alexandrium tamarense from Mikawa Bay, Japan. In: Harmful and Toxic Algal Blooms, Inter–governmental Oceanographic Commission of UNESCO, Yasumoto, T., et al., eds., 293–296.Google Scholar
  90. Zehr, J. P., and Falkowski, P. G., 1988. Pathway of ammonium assimilation in a marine diatom determined with radiotracer 13N1. Journal of Phycology, 24: 588–591.Google Scholar

Copyright information

© Science Press, Ocean University of China and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Xiaoli Jing
    • 1
    • 2
    • 3
  • Tiezhu Mi
    • 2
    • 3
    • 4
    Email author
  • Yu Zhen
    • 2
    • 3
    • 4
  • Hualong Wang
    • 1
    • 2
    • 3
  • Zhigang Yu
    • 2
    • 5
  1. 1.College of Marine Life ScienceOcean University of ChinaQingdaoChina
  2. 2.Function Laboratory for Marine Ecology and Environmental ScienceQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.Key Laboratory of Marine Environment and EcologyMinistry of EducationQingdaoChina
  4. 4.College of Environmental Science and EngineeringOcean University of ChinaQingdaoChina
  5. 5.Key Laboratory of Marine Chemical Theory and TechnologyMinistry of EducationQingdaoChina

Personalised recommendations