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 CONTROL1

The elemental composition and the cell cycle stages of the marine diatom Thalassiosira pseudonana Hasle and Heimdal were studied in continuous cultures over a range of different light‐ (E), nitrogen‐ (N), and phosphorus‐ (P) limited growth rates. In all growth conditions investigated, the decrease in the growth rate was linked with a higher relative contribution of the G2+M phase. The other phases of the cell cycle, G1 and S, showed different patterns, depending on the type of limitation. All experiments showed a highly significant increase in the amount of biogenic silica per cell and per cell surface with decreasing growth rates. At low growth rates, the G2+M elongation allowed an increase of the silicification of the cells. This pattern could be explained by the major uptake of silicon during the G2+M phase and by the independence of this process on the requirements of the other elements. This was illustrated by the elemental ratios Si/C and Si/N that increased from 2‐ to 6‐fold, depending of the type of limitation, whereas the C/N ratio decreased by 10% (E limitation) or increased by 50% (P limitation). The variations of the ratios clearly demonstrate the uncoupling of the Si metabolism compared with the C and N metabolisms. This uncoupling enabled us to explain that in any of the growth condition investigated, the silicification of the cells increased at low growth rates, whereas carbon and nitrogen cellular content are differently regulated, depending of the growth conditions.

[1]  D. Vaulot,et al.  Cell Cycle Regulation by Light inProchlorococcus Strains , 2001, Applied and Environmental Microbiology.

[2]  N. Kröger,et al.  Species-specific polyamines from diatoms control silica morphology. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Mark Hildebrand,et al.  SILICON METABOLISM IN DIATOMS: IMPLICATIONS FOR GROWTH  , 2000 .

[4]  P. Trost,et al.  METABOLIC RESPONSES OF THE DIATOM ACHNANTHES BREVIPES (BACILLARIOPHYCEAE) TO NUTRIENT LIMITATION  , 2000 .

[5]  M. Hildebrand,et al.  NITRATE TRANSPORTER GENES FROM THE DIATOM CYLINDROTHECA FUSIFORMIS (BACILLARIOPHYCEAE): mRNA LEVELS CONTROLLED BY NITROGEN SOURCE AND BY THE CELL CYCLE , 2000, Journal of phycology.

[6]  D. Kreeger,et al.  EFFECT OF NUTRIENT AVAILABILITY ON THE BIOCHEMICAL AND ELEMENTAL STOICHIOMETRY IN THE FRESHWATER DIATOM STEPHANODISCUS MINUTULUS (BACILLARIOPHYCEAE)* , 2000, Journal of phycology.

[7]  M. Brzezinski,et al.  THE CHEMICAL FORM OF DISSOLVED SI TAKEN UP BY MARINE DIATOMS , 1999 .

[8]  N. Kröger,et al.  Polycationic peptides from diatom biosilica that direct silica nanosphere formation. , 1999, Science.

[9]  D. Gradmann,et al.  Electrophysiology of the marine diatom Coscinodiscus wailesii III. Uptake of nitrate and ammonium , 1999 .

[10]  P. Falkowski,et al.  DIEL PERIODICITY OF NITRATE REDUCTASE ACTIVITY AND PROTEIN LEVELS IN THE MARINE DIATOM THALASSIOSIRA WEISSFLOGII (BACILLARIOPHYCEAE) , 1998 .

[11]  M. Sieracki,et al.  CELLULAR DNA CONTENT OF MARINE PHYTOPLANKTON USING TWO NEW FLUOROCHROMES: TAXONOMIC AND ECOLOGICAL IMPLICATIONS 1 , 1997 .

[12]  Mark Hildebrand,et al.  A gene family of silicon transporters , 1997, Nature.

[13]  D. Vaulot,et al.  Effect of phosphorus starvation on the cell cycle of the photosynthetic prokaryote Prochlorococcus spp. , 1996 .

[14]  M. Brzezinski,et al.  SILICON DEPOSITION DURING THE CELL CYCLE OF THALASSIOSIRA WEISSFLOGII (BACILLARIOPHYCEAE) DETERMINED USING DUAL RHODAMINE 123 AND PROPIDIUM IODIDE STAINING 1 , 1994 .

[15]  J. Middelburg,et al.  Rapid analysis of organic carbon and nitrogen in particulate materials , 1994 .

[16]  Lisa M. Graziano,et al.  INDUCTION OF SPECIFIC PROTEINS IN EUKARYOTIC ALGAE GROWN UNDER IRON‐, PHOSPHORUS‐, OR NITROGEN‐DEFICIENT CONDITIONS 1 , 1993 .

[17]  A. Murray,et al.  The Cell Cycle: An Introduction , 1993 .

[18]  D. Turpin.  EFFECTS OF INORGANIC N AVAILABILITY ON ALGAL PHOTOSYNTHESIS AND CARBON METABOLISM , 1991 .

[19]  P. Thompson,et al.  Effects of nutrient and light limitation on the biochemical composition of phytoplankton , 1990, Journal of Applied Phycology.

[20]  D. Turpin,et al.  Interactions between photosynthesis, respiration, and nitrogen assimilation in microalgae , 1988 .

[21]  P. Raimbault,et al.  Diurnal variations of intracellular nitrate storage by marine diatoms: effects of nutritional state , 1987 .

[22]  R. Olson,et al.  Cell-cycle response to nutrient starvation in two phytoplankton species, Thalassiosira weissflogii and Hymenomonas carterae , 1987 .

[23]  R. Olson,et al.  Light and dark control of the cell cycle in two marine phytoplankton species. , 1986, Experimental cell research.

[24]  R. Olson,et al.  Effects of environmental stresses on the cell cycle of two marine phytoplankton species. , 1986, Plant physiology.

[25]  M. Brzezinski,et al.  THE Si:C:N RATIO OF MARINE DIATOMS: INTERSPECIFIC VARIABILITY AND THE EFFECT OF SOME ENVIRONMENTAL VARIABLES 1 , 1985 .

[26]  E. Laws,et al.  Light-, nitrogen-, and phosphorus-limited growth of Phaeodactylum tricornutum Bohlin strain TFX-1: chemical composition, carbon partitioning, and the diel periodicity of physiological processes , 1985 .

[27]  J. Raven.  THE TRANSPORT AND FUNCTION OF SILICON IN PLANTS , 1983 .

[28]  Trevor Platt,et al.  Physiological Bases of Phytoplankton Ecology , 1982 .

[29]  Y. Collos.  Transient situations in nitrate assimilation by marine diatoms. III. short-term uncoupling of nitrate uptake and reduction , 1982 .

[30]  S. Wolfe.  The Biology of the Cell , 1981 .

[31]  E. Laws,et al.  Nutrient‐ and light‐limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean , 1980 .

[32]  E. Paasche,et al.  Silicon content of five marine plankton diatom species measured with a rapid filter method1 , 1980 .

[33]  J. Spudich,et al.  Regulation of the Chlamydomonas cell cycle by light and dark , 1980, The Journal of cell biology.

[34]  P. Harrison,et al.  A BROAD SPECTRUM ARTIFICIAL SEA WATER MEDIUM FOR COASTAL AND OPEN OCEAN PHYTOPLANKTON 1 , 1980 .

[35]  Q. Dortch,et al.  Nitrate reductase and glutamate dehydrogenase activities in Skeletonema costatum as measures of nitrogen assimilation rates , 1979 .

[36]  P. J. Syrett,et al.  Ammonium inhibition of nitrate uptake by the diatom, Phaeodactylum tricornutum , 1979 .

[37]  E. Laws,et al.  STUDIES OF CARBON AND NITROGEN METABOLISM BY THREE MARINE PHYTOPLANKTON SPECIES IN NITRATE‐LIMITED CONTINUOUS CULTURE1, 2 , 1978 .

[38]  P. Harrison,et al.  Marine diatoms grown in chemostats under silicate or ammonium limitation. IV. Transient response of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida to a single addition of the limiting nutrient , 1977 .

[39]  C. Davis.  CONTINUOUS CULTURE OF MARINE DIATOMS UNDER SILICATE LIMITATION. II. EFFECT OF LIGHT INTENSITY ON GROWTH AND NUTRIENT UPTAKE OF SKELETONEMA COSTATUM 1, 2 , 1976 .

[40]  P. Betzer,et al.  Decomposition and analysis of refractory oceanic suspended materials , 1976 .

[41]  C. Davis,et al.  Marine diatoms grown in chemostats under silicate or ammonium limitation. II. Transient response of Skeletonema costatum to a single addition of the limiting nutrient , 1976 .

[42]  R. Eppley,et al.  NITROGEN ASSIMILATION OF AN OCEANIC DIATOM IN NITROGEN‐LIMITED CONTINUOUS CULTURE 1 , 1974 .

[43]  R. Guillard,et al.  Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. , 1962, Canadian journal of microbiology.

[44]  D. Turpin,et al.  Integration of Carbon and Nitrogen Metabolism in Plant and Algal Cells , 1994 .

[45]  P. Tréguer,et al.  Determination of biogenic silica in coastal waters: applicability and limits of the alkaline digestion method , 1994 .

[46]  M. Brzezinski.  Cell-cycle effects on the kinetics of silicic acid uptake and resource competition among diatoms , 1992 .

[47]  M. Brzezinski,et al.  Silicon availability and cell-cycle progression in marine diatoms , 1990 .

[48]  C. Sullivan,et al.  Silicification by diatoms. , 1986, Ciba Foundation symposium.

[49]  M. R. Droop,et al.  25 Years of Algal Growth Kinetics A Personal View , 1983 .

[50]  R. Crawford.  The Siliceous Components of the Diatom Cell Wall and Their Morphological Variation , 1981 .

[51]  P. J. Syrett.  Nitrogen metabolism of microalgae , 1981 .

[52]  B. Volcani,et al.  Silicon in the Cellular Metabolism of Diatoms , 1981 .

[53]  B. Volcani.  Cell Wall Formation in Diatoms: Morphogenesis and Biochemistry , 1981 .

[54]  B. Volcani,et al.  Silicon and Siliceous Structures in Biological Systems , 1981, Springer New York.

[55]  J. C. Goldman.  Physiological Processes, Nutrient Availability, and the Concept of Relative Growth Rate in Marine Phytoplankton Ecology , 1980 .

[56]  M. Perry,et al.  Phosphate utilization by an oceanic diatom in phosphorus limited chemostat culture , 1976 .

[57]  Y. Collos,et al.  Significance of cellular nitrate content in natural populations of marine phytoplankton growing in shipboard cultures , 1976 .

[58]  R. Guillard,et al.  Culture of Phytoplankton for Feeding Marine Invertebrates , 1975 .