Physiological and biochemical responses of Thalassiosira punctigera to nitrate limitation

References

• Allen J.T., Brown L., Sanders R., Moore C.M., Mustard A., Fielding S., Lucas M., Rixen M., Savidge G., Henson S. & Mayor D. 2005. Diatom carbon export enhanced by silicate upwelling in the northeast Atlantic. Nature 437: 728–732. doi: 10.1038/nature03948
   PubMed Web of Science ®Google Scholar
• Augueres A.S. & Loreau M. 2015. Regulation of Redfield ratios in the deep ocean. Global Biogeochemical Cycles 29: 254–266. doi: 10.1002/2014GB005066
   Web of Science ®Google Scholar
• Behrenfeld M.J. 2014. Climate-mediated dance of the plankton. Nature Climate Change 4: 880–887. doi:10.1038/Nclimate2349.
   Web of Science ®Google Scholar
• Berges J.A., Charlebois D.O., Mauzerall D.C. & Falkowski P.G. 1996. Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiology 110: 689–696. doi: 10.1104/pp.110.2.689
   PubMed Web of Science ®Google Scholar
• Biddanda B. & Benner R. 1997. Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnology and Oceanography 42: 506–518. doi: 10.4319/lo.1997.42.3.0506
   Web of Science ®Google Scholar
• Brzezinski M.A. & Nelson D.M. 1995. The annual silica cycle in the Sargasso Sea near Bermuda. Deep Sea Research Part I: Oceanographic Research Papers 42: 1215–1237. doi: 10.1016/0967-0637(95)93592-3
   Web of Science ®Google Scholar
• Carpenter E.J. & Guillard R.R.L. 1971. Intraspecific differences in nitrate half-saturation constants for three species of marine phytoplankton. Ecology 52: 183–185. doi: 10.2307/1934753
   Web of Science ®Google Scholar
• Claquin P., Martin-Jézéquel V., Kromkamp J., Veldhuis M. & Kraay G. 2002. Uncoupling of silicon compared with carbon and nitrogen metabolisms and the role of the cell cycle in continuous cultures of Thalassiosira pseudonana (Bacillariophyceae) under light, nitrogen and phosphorus control. Journal of Phycology 38: 922–930. doi: 10.1046/j.1529-8817.2002.t01-1-01220.x
   Web of Science ®Google Scholar
• Coma R., Ribes M., Serrano E., Jimenez E., Salat J. & Pascual J. 2009. Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proceedings of the National Academy of Sciences 106: 6176–6181. doi: 10.1073/pnas.0805801106
   PubMed Web of Science ®Google Scholar
• Dutkiewicz S., Follows M.J. & Bragg J.G. 2009. Modeling the coupling of ocean ecology and biogeochemistry. Global Biogeochemical Cycles 23. doi:10.1029/2008gb003405.
   Web of Science ®Google Scholar
• Eilers P.H.C. & Peeters J.C.H. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42: 199–215. doi: 10.1016/0304-3800(88)90057-9
   Web of Science ®Google Scholar
• Engel A. 2000. The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (α) during the decline of a diatom bloom. Journal of Plankton Research 22: 485–497. doi: 10.1093/plankt/22.3.485
   Web of Science ®Google Scholar
• Engel A., Goldthwait S., Passow U. & Alldredge A. 2002. Temporal decoupling of carbon and nitrogen dynamics in a mesocosm diatom bloom. Limnology and Oceanography 47: 753–761. doi: 10.4319/lo.2002.47.3.0753
   Web of Science ®Google Scholar
• Falkowski P.G. 2012. Ocean science: The power of plankton. Nature 483:S17–S20. doi: 10.1038/483S17a
   PubMed Web of Science ®Google Scholar
• Falkowski P.G., Barber R.T. & Smetacek V. 1998. Biogeochemical controls and feedbacks on ocean primary production. Science 281: 200–206. doi: 10.1126/science.281.5374.200
   PubMed Web of Science ®Google Scholar
• Falkowski P.G. & Raven J.A. 2007. An introduction of photosynthesis in aquatic system. In: Aquatic photosynthesis, 2 edn., p. 1. Princeton: Princeton University Press.
   Google Scholar
• Firme G.F., Rue E.L., Weeks D.A., Bruland K.W. & Hutchins D.A. 2003. Spatial and temporal variability in phytoplankton iron limitation along the California coast and consequences for Si, N, and C biogeochemistry. Global Biogeochemical Cycles 17: 1–13. doi: 10.1029/2001GB001824
   Web of Science ®Google Scholar
• Flynn K.J. & Martin-Jézéquel V. 2000. Modelling Si–N-limited growth of diatoms. Journal of Plankton Research 22: 447–472. doi: 10.1093/plankt/22.3.447
   Web of Science ®Google Scholar
• Geider R. & La Roche J.L. 2002. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. European Journal of Phycology 37: 1–17. doi: 10.1017/S0967026201003456
   Web of Science ®Google Scholar
• Goldman J.C., McCarthy J.J. & Peavey D.G. 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210–215. doi: 10.1038/279210a0
   Web of Science ®Google Scholar
• Goldman J.C., Hansell D.A. & Dennett M.R. 1992. Chemical characterization of three large oceanic diatoms: potential impact on water column chemistry. Marine Ecology Progress Series 88: 257–270. doi: 10.3354/meps088257
   Web of Science ®Google Scholar
• Griffiths M.J., Van Hille R.P. & Harrison S.T.L. 2012. Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applied Phycology 24: 989–1001. doi: 10.1007/s10811-011-9723-y
   Web of Science ®Google Scholar
• Jetten M.S. 2008. The microbial nitrogen cycle. Environmental Microbiology 10: 2903–2909. doi: 10.1111/j.1462-2920.2008.01786.x
   PubMed Web of Science ®Google Scholar
• Jiang Y., Yoshida T. & Quigg A. 2012. Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiology and Biochemistry 54: 70–77. doi: 10.1016/j.plaphy.2012.02.012
   PubMed Web of Science ®Google Scholar
• Jin P., Gao K. & Beardall J. 2013. Evolutionary responses of a Coccolithophorid Gephyrocapsa Oceanica to ocean acidification. Evolution 67: 1869–1878. doi: 10.1111/evo.12112
   PubMed Web of Science ®Google Scholar
• John E.H. & Davidson K. 2001. Prey selectivity and the influence of prey carbon:nitrogen ratio on microflagellate grazing. Journal of Experimental Marine Biology and Ecology 260:93–111. doi: 10.1016/S0022-0981(01)00244-1
   PubMed Web of Science ®Google Scholar
• Laws E.A. 1991. Photosynthetic quotients, new production and net community production in the open ocean. Deep Sea Research Part A. Oceanographic Research Papers 38: 143–167. doi: 10.1016/0198-0149(91)90059-O
   Web of Science ®Google Scholar
• Levitus S., Conkright M.E., Reid J.L., Najjar R.G. & Mantyla A. 1993. Distribution of nitrate, phosphate and silicate in the world oceans. Progress in Oceanography 31: 245–273. doi: 10.1016/0079-6611(93)90003-V
   Web of Science ®Google Scholar
• Levitus S., Antonov J.I., Boyer T.P. & Stephens C. 2000. Warming of the world ocean. Science 287: 2225–2229. doi: 10.1126/science.287.5461.2225
   Web of Science ®Google Scholar
• Li G. & Campbell D.A. 2017. Interactive effects of nitrogen and light on growth rates and RUBISCO content of small and large centric diatoms. Photosynthesis Research 131: 93–103. doi: 10.1007/s11120-016-0301-7
   PubMed Web of Science ®Google Scholar
• Li W., Gao K. & Beardall J. 2012. Interactive effects of ocean acidification and nitrogen-limitation on the diatom phaeodactylum tricornutum. PLoS One 7: e51590. doi:doi: 10.1371/journal.pone.0051590.
   PubMed Web of Science ®Google Scholar
• Li W., Gao K. & Beardall J. 2015. Nitrate limitation and ocean acidification interact with UV-B to reduce photosynthetic performance in the diatom Phaeodactylum tricornutum. Biogeosciences (online) 12: 2383–2393. doi: 10.5194/bg-12-2383-2015
   Web of Science ®Google Scholar
• Litchman E., Klausmeier C.A., Schofield O.M. & Falkowski P.G. 2007. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecology Letters 10: 1170–1181. doi: 10.1111/j.1461-0248.2007.01117.x
   PubMed Web of Science ®Google Scholar
• Liu W.H., Huang Z.W., Li P., Xia J.F. & Chen B. 2012. Formation of triacylglycerol in Nitzschia closterium f. minutissima under nitrogen limitation and possible physiological and biochemical mechanisms. Journal of Experimental Marine Biology and Ecology 418-419: 24–29. doi: 10.1016/j.jembe.2012.03.005
   Web of Science ®Google Scholar
• Mei Z.P., Finkel Z.V. & Irwin A.J. 2009. Light and nutrient availability affect the size-scaling of growth in phytoplankton. Journal of Theoretical Biology 259: 582–588. doi: 10.1016/j.jtbi.2009.04.018
   PubMed Web of Science ®Google Scholar
• Monod J. 1950. The technique, theory and applications of continuous culture. Annales de I'Institut Pasteur 79: 184–204.
   Google Scholar
• Moore C.M., Mills M.M., Langlois R., Milne A., Achterberg E.P., La Roche J. & Geider R.J. 2008. Relative influence of nitrogen and phosphorous availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical north Atlantic Ocean. Limnology and Oceanography 53: 291–305. doi: 10.4319/lo.2008.53.1.0291
   Web of Science ®Google Scholar
• Morel F.M., Rueter J., Anderson D.M. & Guillard R. 1979. Aquil: a chemically defined phytoplankton culture medium for trace metal studies. Journal of Phycology 15: 135–141. doi: 10.1111/j.0022-3646.1979.00135.x
   Web of Science ®Google Scholar
• Mutshinda C.M., Finkel Z.V., Widdicombe C.E. & Irwin A.J. 2017. Phytoplankton traits from long-term oceanographic time-series. Marine Ecology Progress Series 576: 11–25. doi:doi: 10.3354/meps12220.
   Web of Science ®Google Scholar
• Nelson D.M., Treguer P., Brzezinski M.A., Leynaert A. & Queguiner B. 1995. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles 9: 359–372. doi: 10.1029/95GB01070
   Web of Science ®Google Scholar
• Palter J. 2015. Storms bring ocean nutrients to light. Nature 525: 460–461. doi: 10.1038/525460a
   PubMed Web of Science ®Google Scholar
• Ragueneau O., Tréguer P., Leynaert A., Anderson R., Brzezinski M., Demaster D., Dugdale R., Dymond J., Fischer G. & Francois R. 2000. A review of the Si cycle in the modern ocean: recent progress and missing gaps in the application of biogenic opal as a paleoproductivity proxy. Global and Planetary Change 26: 317–365. doi: 10.1016/S0921-8181(00)00052-7
   Web of Science ®Google Scholar
• Redfield A.C. 1958. The biological control of chemical factors in the environment. American Scientist 46:205–221.
   Web of Science ®Google Scholar
• Ritchie R.J. 2006. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynthesis Research 89: 27–41. doi: 10.1007/s11120-006-9065-9
   PubMed Web of Science ®Google Scholar
• Rykaczewski R.R. & Dunne J.P. 2010. Enhanced nutrient supply to the California current ecosystem with global warming and increased stratification in an earth system model. Geophysical Research Letters 37: 5. doi:doi: 10.1029/2010gl045019.
   Web of Science ®Google Scholar
• Sarthou G., Timmermans K.R., Blain S. & Treguer P. 2005. Growth physiology and fate of diatoms in the ocean: a review. Journal of Sea Research 53: 25–42. doi: 10.1016/j.seares.2004.01.007
   Web of Science ®Google Scholar
• Schartau M., Engel A., Schröter J., Thoms S., Völker C. & Wolf-Gladrow D. 2007. Modelling carbon overconsumption and the formation of extracellular particulate organic carbon. Biogeosciences (online) 4: 433–454. doi:doi: 10.5194/bg-4-433-2007.
   Web of Science ®Google Scholar
• Sigmon D.E., Nelson D.M. & Brzezinski M.A. 2002. The Si cycle in the pacific sector of the Southern Ocean: seasonal diatom production in the surface layer and export to the deep sea. Deep Sea Research Part II: Topical Studies in Oceanography 49: 1747–1763. doi: 10.1016/S0967-0645(02)00010-3
   Web of Science ®Google Scholar
• Siuda A.N. & Dam H.G. 2010. Effects of omnivory and predator-prey elemental stoichiometry on planktonic trophic interactions. Limnology and Oceanography 55:2107–2116. doi: 10.4319/lo.2010.55.5.2107
   Web of Science ®Google Scholar
• Smetacek V. 1999. Diatoms and the ocean carbon cycle. Protist 150: 25–32. doi: 10.1016/S1434-4610(99)70006-4
   PubMed Web of Science ®Google Scholar
• Sterner R.W., Clasen J., Lampert W. & Weisse T. 1998. Carbon:phosphorus stoichiometry and food chain production. Ecology Letters 1: 146–150. doi: 10.1046/j.1461-0248.1998.00030.x
   Web of Science ®Google Scholar
• Sun H.F., Wang H.W. & Yuan C.Y. 2014. Optimization of zinc-cadmium reduction method for determination of nitrate in seawater. In: Environmental engineering, Pts 1-4, vol 864-867. (Ed. by H. Li, Q. Xu & H. Ge), pp. 1004–1007. Advanced Materials Research. Trans Tech Publications Ltd, Stafa-Zurich.
   Google Scholar
• Talarmin A., Lomas M.W., Bozec Y., Savoye N., Frigstad H., Karl D.M. & Martiny A.C. 2016. Seasonal and long-term changes in elemental concentrations and ratios of marine particulate organic matter. Global Biogeochemical Cycles 30: 1699–1711. doi: 10.1002/2016GB005409
   Web of Science ®Google Scholar
• Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525–531. doi: 10.1038/22941
   Web of Science ®Google Scholar
• Vitousek P. & Howarth R. 1991. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13: 87–115. doi: 10.1007/BF00002772
   Web of Science ®Google Scholar
• Wang J.H., Tang H.J., Yang R.J. & Wang X.L. 2008. The effects of nitrate and phosphate on the growth and nitrate reductase activity of Skeletonema costatum. Marine Sciences 32: 64–68.
   Google Scholar
• Woodland R.J., Thomson J.R., Mac Nally R., Reich P., Evrard V., Wary F.Y., Walker J.P. & Cook P.L.M. 2015. Nitrogen loads explain primary productivity in estuaries at the ecosystem scale. Limnology and Oceanography 60: 1751–1762. doi: 10.1002/lno.10136
   Web of Science ®Google Scholar
• Wu Y., Campbell D.A., Irwin A.J., Suggett D.J. & Finkel Z.V. 2014a. Ocean acidification enhances the growth rate of larger diatoms. Limnology and Oceanography 59: 1027–1034. doi: 10.4319/lo.2014.59.3.1027
   Web of Science ®Google Scholar
• Wu Y., Jeans J., Suggett D., Finkel Z. & Campbell D.A. 2014b. Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates. Frontiers in Marine Science 1: 68. doi:doi: 10.3389/fmars.2014.00068.
   Google Scholar
• Xiao W., Liu X., Irwin A.J., Laws E., Wang L., Chen B., Zeng Y. & Huang B. 2018. Warming and eutrophication combine to restructure diatoms and dinoflagellates. Water Research 128: 206–216. doi:10.1016/j.watres.2017.10.051.
   PubMed Web of Science ®Google Scholar
• Yool A. & Tyrrell T. 2003. Role of diatoms in regulating the ocean’s silicon cycle. Global Biogeochemical Cycles 17: 1–21. doi: 10.1029/2002GB002018
   Web of Science ®Google Scholar