Skip to main content
Log in

Regulation of the Si and C uptake and of the soluble free-silicon pool in a synchronised culture of Cylindrotheca fusiformis (Bacillariophyceae): effects on the Si/C ratio

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Silicon and carbon uptake rates were studied over a 24 h light/dark cycle in a synchronised culture of the marine diatom Cylindrotheca fusiformis (Reimann et Lewin) using 32Si and 14C. The silicic acid uptake rate per cell (ρcSi) varied between 1.2 and 20.0 fmol Si cell−1 h−1 and was closely correlated to the G2+M phase of the cell cycle. A linear and significant relationship was determined between the percentage of cells present in G2+M and ρcSi. Evolution of the soluble free-silicon pool was studied simultaneously. The concentration of the total soluble free pool of silicon (QPSi) varied from 1% to 7% of the total silicon content. A significant difference of 1.5 fmol Si cell−1 between QPSi and the labelled free pool (QnpSi) was measured, indicating the presence of an unlabelled fraction of the pool. The concentration of QnpSi was around 1.0 fmol Si cell−1 prior to cell division and did not change as a function of ρcSi, which indicated a feedback mechanism coupling uptake into the free pool and incorporation into the frustule. In parallel, 14C uptake variation (ρcC) was measured during the division of the population. The value of ρcC varied between 0.44 and 0.78 pmol C cell−1 h−1 and appeared to be maximal when cells were in the G1 phase. This variation of ρcC marginally affected the total carbon content of the cells (QTC) in comparison with the light/dark cycle. The variations in the Si/C ratio, from 0.021 to 0.046, demonstrated the different control mechanisms of Si and C metabolisms during the course of the cell- and photocycle.

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

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    CAS  PubMed  Google Scholar 

  • Azam F, Hemmingsen BB, Volcani BE (1974) Role of silicon in diatom metabolism. V. Silicic acid transport and metabolism in the heterotrophic diatom Nitzschia alba. Arch Microbiol 97:103–114

    Article  CAS  PubMed  Google Scholar 

  • Binder BJ, Chisholm SW (1980) Changes in the soluble silicon pool size in the marine diatom Thalassisira weisflogii. Mar Biol Lett 1:205–212

    Google Scholar 

  • Brzezinski MA (1985) The Si:C:N ratio of the marine diatoms: interspecific variability and the effect of some environmental variables. J Phycol 21:347–357

    CAS  Google Scholar 

  • Brzezinski MA (1992) Cell-cycle effects on the kinetics of silicic acid uptake and resource competition among diatoms. J Plankton Res 14:1511–1539

    CAS  Google Scholar 

  • Brzezinski MA, Olson RJ, Chisholm SW (1990) Silicon availability and cell-cycle progression in marine diatoms. Mar Ecol Prog Ser 67:83–96

    CAS  Google Scholar 

  • Brzezinski MA, Dickson ML, Nelson DM, Sambrotto R (2003) Ratio of Si, C and N uptake by microplankton in the Southern Ocean. Deep-Sea Res Part II 50:619–633

    Google Scholar 

  • Busby WF, Lewin JC (1967) Silicate uptake and silica shell formation by synchronously dividing cells of the diatom Navicula pelliculosa (Breb) Hilse. J Phycol 3:127–131

    Google Scholar 

  • Chisholm SW (1981) Temporal patterns of cell division in unicellular algae. In: Platt T (ed) Physiological bases of phytoplankton ecology. Can Bull Fish Aquat Sci 210:150–181

    Google Scholar 

  • Chisholm SW, Azam F, Eppley RW (1978) Silicic acid incorporation in marine diatoms on light:dark cycles: use as an essay for phased cell division. Limnol Oceanogr 23:518–529

    CAS  Google Scholar 

  • Claquin P, Martin-Jézéquel V, Kromkamp JC, Veldhuis MJW, Kraay GW (2002) Uncoupling of silicon compared to carbon and nitrogen metabolism, and role of the cell cycle, in continuous cultures of Thalassiosira pseudonana (Bacillariophyceae) under light, nitrogen and phosphorus control. J Phycol 38:922–930

    Article  CAS  Google Scholar 

  • Claquin P, Kromkamp JC, Martin-Jézéquel V (2004) Relationship between photosynthetic metabolism and cell cycle in a synchronized culture of the marine alga Cylindrotheca fusiformis (Bacillariophyceae). Eur J Phycol 39:33–41

    Article  CAS  Google Scholar 

  • Conway HL, Harrison PJ (1977) 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. Mar Biol 43:33–43

    Article  CAS  Google Scholar 

  • Conway HL, Harrison PJ, Davis CO (1976) Marine diatoms grown in chemostats under silicate or ammonium limitation. II. Transient response of Skeletonema costatum to a single addition of the limiting nutrient. Mar Biol 35:187–199

    Article  CAS  Google Scholar 

  • Cuhel RL, Ortner PB, Lean DRS (1984) Night synthesis of protein by algae. Limnol Oceanogr 29:731–744

    CAS  Google Scholar 

  • Darley WM, Sullivan CW, Volcani BE (1976) Studies on the biochemistry and fine structure of silica shell formation in diatoms, division cycle and chemical composition of Navicula pelliculosa during light–dark synchronized growth. Planta 130:159–167

    Article  CAS  Google Scholar 

  • Davis CO (1976) Continuous culture of marine diatoms under silicate limitation. II. Effect of light intensity on growth and nutrient uptake of Skeletonema costatum. J Phycol 12:291–300

    CAS  Google Scholar 

  • Eggimann DW, Betzer PR (1976) Decomposition and analysis of refractory suspended material. Anal Chem 48:1886–1890

    Google Scholar 

  • Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell Science, Malden, USA

  • Fitzwater SE, Knauer GA, Martin JH (1982) Metal contamination and its effects on primary production. Limnol Oceanogr 27:544–551

    CAS  Google Scholar 

  • Flynn KJ, Martin-Jézéquel V (2000) Modelling Si-N-limited growth of diatoms. J Plankton Res 22:447–472

    Article  CAS  Google Scholar 

  • Gensemer RW (1990) Role of aluminium and growth rate on changes in cell size and silica content of silica-limited populations of Asterionnella ralfsii var. americana (Bacillariophyceae). J Phycol 26:250–258

    Article  CAS  Google Scholar 

  • Gordon LI, Jennings JC, Ross AA, Krest JM (1992) A suggested protocol for continuous flow automated analysis of seawater nutrients in the WOCE hydrographic programme and the JGOFS study. Technical report no. 92-1, College of Oceanography, Oregon State University, Corvallis, Ore., USA

  • Gordon R, Drum RW (1994) The chemical basis of diatom morphogenis. Int Rev Cytol 150:243–372

    CAS  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum, New York, pp 26–60

    Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    CAS  PubMed  Google Scholar 

  • Harrison PJ, Conway HL, Dugdale RC (1976) Marine diatoms grown in chemostats under silicate or ammonium limitation. I. Cellular chemical composition and steady-state growth kinetics of Skeletonema costatum. Mar Biol 35:177–186

    Article  CAS  Google Scholar 

  • Harrison PJ, Conway HL, Holmes RW, Davis CO (1977) Marine diatoms grown in chemostats under silicate or ammonium limitation. III. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum and Thalassiosira gravida. Mar Biol 43:19–31

    CAS  Google Scholar 

  • Harrison PJ, Waters RE, Taylor FJR (1980) A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton. J Phycol 16:28–35

    Google Scholar 

  • Heil WG, Senger H (1986) Thylakoid-protein phosphorylation during the life cell of Scenedesmus obliquus in synchronous culture. Planta 167:233–239

    Article  CAS  Google Scholar 

  • Hildebrand M (2000) Silicic acid transport and its control during cell wall silicification in diatoms. In: Bauerlein E (ed) Biomineralization of nano- and micro-structures Wiley-VCH, Weinheim, Germany, pp 171–188

  • Hildebrand M, Wetherbee R (2003) Components and control of silicification in diatoms. In: Mueller WEG (ed) Silicon biomineralization: biology, biochemistry, molecular biology, biotechnology. Progress in molecular and subcellular biology, vol 33. Springer, Heidelberg Berlin New York, pp 11–57

  • Hildebrand M, Volcani BE, Gassman W, Schroeder JI (1997) A gene family of silicon transporters. Nature 385:688–689

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand M, Dahlin K, Volcani BE (1998) Characterization of a silicon transporter gene family in Cylindrotheca fusiformis: sequences, expression analysis, and identification of homologs in other diatoms. Mol Gen Genet 260:480–486

    Article  CAS  PubMed  Google Scholar 

  • Kaftan D, Meszaros T, Whitmarsh J, Nedbal L (1999) Characterization of photosystem II activity and heterogeneity during the cell cycle of the green alga Scenedesmus quadricauda. Plant Physiol (Rockv) 120:433–441

    Google Scholar 

  • Kinrade SD, Gillson A-ME, Knight CTG (2002) Silicon-29 NMR evidence of a transient hexavalent silicon complex in the diatom Navicula pelliculosa. J Chem Soc Dalton Trans 3:307–309

    Article  Google Scholar 

  • Lewis MR, Smith JC (1983) A small volume short-incubation-time method for measurement of photosynthesis as a function of incident irradiance. Mar Ecol Prog Ser 13:99–102

    CAS  Google Scholar 

  • Leynaert A, Tréguer P, Nelson DM, Del Amo Y (1996) 32Si as a tracer of biogenic silica production: methodological improvements. In: Baeyens J, Dehairs F, Goeyens L (eds) Integrated marine system analysis, minutes of the first workshop meeting. VUB, Brussels, Belgium, pp 29–35

  • Leynaert A, Bucciarelli E, Claquin P, Dugdale RC, Martin-Jézéquel V, Pondaven P, Ragueneau O (2004) Effect of iron deficiency on diatom cell size and on silicic acid uptake kinetics. Limnol Oceanogr 49:1134–1143

    CAS  Google Scholar 

  • Martin-Jézéquel V, Lopez PJ (2003) Silicon a central metabolite for growth and morphogenesis. In: Müller WEG (ed) Silicon biomineralization: biology, biochemistry, molecular biology, biotechnology. Progress in molecular and subcellular biology, vol 33. Springer, Heidelberg Berlin New York, pp 99–124

  • Martin-Jézéquel V, Hildebrand M, Brzezinski MA (2000) Silicon metabolism in diatoms: implications for growth. J Phycol 36:821–840

    Article  Google Scholar 

  • Milligan AJ, Varela DE, Brzezinski MA, Morel FMM (2004) Dynamics of silicon metabolism and silicon isotopic discrimination in a marine diatom as a function of pCO2. Limnol Oceanogr 49:322–329

    CAS  Google Scholar 

  • Mitchison JM (1971) The biology of the cell. Cambridge University Press, Cambridge

  • Mullin JB, Riley JP (1965) The spectrometric determination of silicate-silicon in natural waters with special reference to sea water. Anal Chem 46:491–501

    Google Scholar 

  • Nieuwenhuize J, Maas YEM, Middelburg JJ (1994) Rapid analyses of organic carbon and nitrogen in particulate materials. Mar Chem 44:217–224

    Article  Google Scholar 

  • Olson RJ, Vaulot D, Chisholm SW (1986) Effects of environmental stresses on the cell cycle of two marine phytoplankton species. Plant Physiol (Rockv) 80:918–925

    Google Scholar 

  • Paasche E (1980) Silicon content of five marine plankton diatom species measured with a rapid filter method. Limnol Oceanogr 25:474–480

    CAS  Google Scholar 

  • Penna A, Magnani M, Fenoglio I, Fubini B, Cerrano C, Giovine M, Bavestrello G (2003) Marine diatom growth on different forms of particulate silica: evidence of cell/particle interaction. Aquat Microb Ecol 32:299–306

    Google Scholar 

  • Pickett-Heaps J, Schmid A-MM, Edgar LA (1990) The cell biology of diatom valve formation. Prog Phycol Res 7:1–168

    Google Scholar 

  • Planchais S, Glab N, Inzé D, Bergounioux C (2000) Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 476:78–83

    Article  CAS  PubMed  Google Scholar 

  • Post AF, Dubinsky Z, Wyman K, Falkowski PG (1985a) Physiological responses of a marine planktonic diatom to transitions in growth irradiance. Mar Ecol Prog Ser 25:141–149

    CAS  Google Scholar 

  • Post AF, Eijgenraam F, Mur LR (1985b) Influence of light period length on photosynthesis and synchronous growth of the green alga Scenedesmus protuberans. Br Phycol J 20:391–397

    Google Scholar 

  • Prézelin BB (1992) Diel periodicity in phytoplankton productivity. Hydrobiologia 238:1–35

    Google Scholar 

  • Ragueneau O, Treguer P (1994) Determination of biogenic silica in coastal waters: applicability and limits of alkaline digestion method. Mar Chem 45:43–51

    Article  CAS  Google Scholar 

  • Ragueneau O, Dittert N, Pondaven P, Tréguer P, Corrin L (2002) Si/C decoupling in the world ocean: is the Southern Ocean different? Deep-Sea Res II 49:3127–3154

    Google Scholar 

  • Raven JA (1983) The transport and function of silicon in plants. Biol Rev 58:178–207

    Google Scholar 

  • Reimann BEF (1964) Deposition of silica inside a diatom cell. Exp Cell Res 34:605–608

    CAS  PubMed  Google Scholar 

  • Reimann BEF, Lewin JC, Volcani BE (1965) Studies on the biochemistry and fine structure of the silica shell formation in diatoms. I. The structure of the cell wall of Cylindrotheca fusiformis Reimann and Lewis. J Cell Biol 24:39–55

    Article  CAS  PubMed  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms, biology and morphology of the genera. Cambridge University Press, Cambridge

  • Sorokin C (1957) Changes in photosynthetic activity in the course of cell development in Chlorella. Physiol Plant 10:659–666

    CAS  Google Scholar 

  • Strasser BJ, Dau H, Heinze I, Senger H (1999) Comparison of light induced and cell cycle dependent changes in the photosynthetic apparatus: a fluorescence induction study on the green alga Scenedesmus obliquus. Photosynth Res 60:217–227

    Article  CAS  Google Scholar 

  • Strickland JD, Parsons TR (1972) A practical handbook of water analysis. Bull Fish Res Board Can 167:310–311

    Google Scholar 

  • Sullivan CW (1976) Diatom mineralization of silicic acid. I. Si(OH)4 transport characteristics in Navicula pelliculosa. J Phycol 12:390–396

    CAS  Google Scholar 

  • Sullivan CW (1977) Diatom mineralization of silicic acid. II. Si(OH)4 transport rate during the cell cycle of Navicula pelliculosa. J Phycol 13:86–91

    CAS  Google Scholar 

  • Sullivan CW (1979) Diatom mineralization of silicic acid. IV. Kinetics of soluble Si pool formation in exponentially growing and synchronized Navicula pelliculosa. J Phycol 15:210–216

    CAS  Google Scholar 

  • Sullivan CW (1980) Diatom mineralization of silicic acid. V. Energetic and macromolecular requirements for Si(OH)4 mineralization events during the cell cycle of Navicula pelliculosa. J Phycol 16:321–328

    CAS  Google Scholar 

  • Sullivan CW (1986) Silicification by diatoms. In: Evered D, O’Connor M (eds) Silicon biochemistry. Ciba foundation symposium 121, Wiley Interscience, Chichester, pp 59–89

  • Sullivan CW, Volcani BE (1981) Silicon in the cellular metabolism of diatoms. In: Simpson TL, Volcani BE (eds) Silicon and siliceous structures in biological systems. Springer, New York Heidelberg Berlin, pp 15–42

  • Szurkowski J, Bascik-Remisiewicz A, Matusiak K, Tukaj Z (2001) Oxygen evolution and photosynthetic energy storage during the cell cycle of green alga Scenedesmus armatus characterized by phoacoustic spectroscopy. J Plant Physiol 158:1061–1067

    CAS  Google Scholar 

  • Taylor NJ (1985) Silica incorporation in the diatom Coscinodiscus granii as affected by light intensity. Br Phycol J 20:365–374

    Google Scholar 

  • Terry KL (1982) Nitrate uptake and assimilation in Thalassiosira weissflogii and Phaeodactylum tricornutum: interaction with photosynthesis and with the uptake of other ions. Mar Biol 69:21–30❚

    Article  CAS  Google Scholar 

  • Turpin DH, Elrifi IR, Birch DG, Weger HG, Holmes JJ (1988) Interactions between photosynthesis, respiration, and nitrogen assimilation in microalgae. Can J Bot 66:2083–2097

    CAS  Google Scholar 

  • Vaulot D, Chisholm SW (1987) A simple model of the growth of phytoplankton populationsin light/dark cycles. J Plankton Res 9:345–366

    Google Scholar 

  • Veldhuis MJW, Cucci TL, Sieracki ME (1997) Cellular DNA content of marine phytoplankton using two new fluorochromes: taxonomic and ecological implications. J Phycol 33:527–541

    Article  CAS  Google Scholar 

  • Volcani BE (1981) Cell wall formation in diatoms: morphogenesis and biochemistry. In: Simpson TL, Volcani BE (eds) Silicon and siliceous structures in biological systems. Springer, New York Heidelberg Berlin, pp 157–200

  • Vrieling EG, Gieskes WWC, Beelen TPM (1999a) Silicon deposition in diatoms: control by the pH inside the silicon deposition vesicle. J Phycol 35:548–559

    Article  CAS  Google Scholar 

  • Vrieling EG, Poort L, Beelen TPM, Gieskes WWC (1999b) Growth and silica content of the diatoms Thalassiosira weissflogii and Navicula salinarum at different salinities and enrichments with aluminium. Eur J Phycol 34:307–316

    Article  Google Scholar 

  • Winter J, Brandt P (1986) Stage-specific state I-state transitions during the cell cycle of Euglena gracilis. Plant Physiol (Rockv) 81:548–552

    Google Scholar 

Download references

Acknowledgements

This work was supported by the CNRS, the Université de Bretagne Occidentale and the Conseil Régional de Bretagne. We are grateful to Dr L. Aude for advice about 32Si experiments, to Le Loch François for technical assistance and to I. Probert for his help with English corrections.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Claquin.

Additional information

Communicated by S.A. Poulet, Roscoff

Rights and permissions

Reprints and permissions

About this article

Cite this article

Claquin, P., Martin-Jézéquel, V. Regulation of the Si and C uptake and of the soluble free-silicon pool in a synchronised culture of Cylindrotheca fusiformis (Bacillariophyceae): effects on the Si/C ratio. Marine Biology 146, 877–886 (2005). https://doi.org/10.1007/s00227-004-1493-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-004-1493-5

Keywords

Navigation