Photosynthesis Research

, Volume 95, Issue 1, pp 37–44 | Cite as

Photosynthetic oscillation in individual cells of the marine diatom Coscinodiscus wailesii (Bacillariophyceae) revealed by microsensor measurements

Research Article

Abstract

Oscillations with a period of 1–2 min in the rate of photosynthesis have been found in leaves of C3 and C4 land plants under invariant, saturating, light and carbon dioxide. This article reports the occurrence of similar oscillations with a period of 2–2.5 min in individual cells of the marine diatom Coscinodiscus wailesii. These oscillations were determined by measurements of both oxygen (oxygen microelectrode) and carbon dioxide (pH microelectrode) just outside the plasmalemma. These oscillations were found in less than 1% of the cells examined. The occurrence of oscillations in unicelluar diatoms rules out for these organisms hypotheses as to the origin of oscillations in land plant leaves that are based on cell–cell interactions.

Keywords

Coscinodiscus wailesii Diatom Photosynthetic oscillation 

Abbreviations

CA

Carbonic anhydrase

CCM

Carbon concentrating mechanism

CO2

Carbon dioxide

CO32-

Carbonate anion

HCO3

Bicarbonate

O2

Oxygen

Notes

Acknowledgements

SK is very grateful to Stephanie Köhler-Rink (Max Planck Institute for Marine Microbiology, Bremen) who not only shared her knowledge on microsensors but also her workplace in the laboratory. JAR acknowledges support from NERC for work on algal photosynthesis.

References

  1. Andrianov VK, Kurella GA, Litvin FF (1965) Changes of resting potential of alga Nitella cells and the connection of this effect with photosynthesis. Biophysics 10:588–591Google Scholar
  2. Anning K, Nimer CA, Merrett MJ, Brownlee C (1996) Costs and benefits of calcification in coccolithophorids. J Mar Sys 9:45–56CrossRefGoogle Scholar
  3. Brehm-Stecher BF, Johnson EA (2004) Single-cell microbiology:tools, technologies, and applications. Microbiol Mol Biol Rev 68:538–559PubMedCrossRefGoogle Scholar
  4. Boyd CM, Gradmann D (1999) Electrophysiology of the diatom Coscinodiscus wailesii. I. Endogenous changes of membrane voltage and resistance. J exp Bot 50:445–452CrossRefGoogle Scholar
  5. Burkhardt S, Riebesell U, Zondervan I (1999) Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochimica et Cosmochimica Acta 63:3729–3741CrossRefGoogle Scholar
  6. Burns BD, Beardall J (1987) Utilization of inorganic carbon by marine microalgae. J Exp Mar Biol Ecol 107:75–86CrossRefGoogle Scholar
  7. Chen CY, Durbin ED (1994) Effects of pH on the growth and carbon uptake of marine phytoplankton. Mar Ecol Prog Ser 109:83–94CrossRefGoogle Scholar
  8. Colman B, Rotatore C (1995) Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant, Cell Environ 18:919–924CrossRefGoogle Scholar
  9. de Beer D, Glud A, Epping E, Kühl M (1997) A fast responding CO2 microelectrode for profiling in sediments, microbial mats and biofilms. Limnol Oceanogr 42:1590–1600CrossRefGoogle Scholar
  10. Eisensamer B, Roennenberg T (2004) Extracellular pH is under circadian control in Gonyaulax polyedra and forms a metabolic feedback loop. Chronobiol Int 21:27–41PubMedCrossRefGoogle Scholar
  11. Endo R, Omasa K (2004) Chlorophyll fluorescence imaging of individual algal cells:effect of herbicide on Spirogyra distentata at different growth stages. Environ Sci Technol 38:4165–4168PubMedCrossRefGoogle Scholar
  12. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, NJ, USAGoogle Scholar
  13. Ferimazova N, Küpper H, Nedbal L, Trtilek M (2002) New insights into photosynthetic oscillations revealed by two-dimensional microscopic measurements of chlorophyll fluorescence kinetics in intact leaves and isolated protoplasts. Photochem photobiol 76:501–508PubMedCrossRefGoogle Scholar
  14. Goldman JC (1999) Inorganic carbon availability and the growth of large marine diatoms. Mar Ecol Prog Ser 180:81–91CrossRefGoogle Scholar
  15. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. Can J Microbiol 8:229–239PubMedGoogle Scholar
  16. Hansen PJ (2002) Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat Microb Ecol 28:279–288CrossRefGoogle Scholar
  17. Hansen U-P, Gradmann D (1971) The action of sinusoidally modulated light on the membrane potential of Acetabularia. Plant Cell Physiol 12:335–348Google Scholar
  18. Hansen U-P, Kolbowski J, Dau H (1987) Relationship between photosynthesis and plasmalemma transport. J exp Bot 38:1965–1981CrossRefGoogle Scholar
  19. Kesseler H (1967) Untersuchungen über die chemische Zusammensetzung des Zellsaftes der Diatomee Coscinodiscus wailesii (Bacillariophyceae, Centrales). Helgoländer wiss Meeresunters 16:262–270CrossRefGoogle Scholar
  20. Köhler-Rink S, Kühl M (2000) Microsensor studies of photosynthesis and respiration in larger symbiotic foraminifera. I The physico–chemical microenvironment of Marginopora vertebratis, Amphistegina lobifera and Amphisorus hemperichii. Mar Biol 137:473–486CrossRefGoogle Scholar
  21. Korb RE, Saville PJ, Johnston AM, Raven JA (1997) Sources of inorganic carbon for photosynthesis by three species of marine diatom. J Phycol 33:433–440CrossRefGoogle Scholar
  22. Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  23. Kühn SF, Brownlee C (2005) Membrane organisation and dynamics in the marine diatom Coscinodiscus wailesii (Bacillariophyceae). Bot Mar 48:297–305CrossRefGoogle Scholar
  24. Kühn SF, Köhler-Rink S (submitted) pH effect on the susceptibility to parasitoid infection in the marine diatom Coscinodiscus spp. (Bacillariophyceae). Mar BiolGoogle Scholar
  25. Laisk A, Siebke K, Gerst U, Eichelmann H, Oja V, Heber U (1991) Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. Planta 185:75–86 CrossRefGoogle Scholar
  26. Nimer NA, Iglesias-Rodriguez MD, Merrett MJ (1997) Bicarbonate utilization by marine phytoplankton species. J Phycol 33:625–631 CrossRefGoogle Scholar
  27. Oxborough K, Hanlon ARM, Underwood GJC, Baker NR (2000) In vivo estimation of the photosystem II photochemical efficiency of individual microphytobenthic cells using high-resolution imaging of chlorophyll a fluorescence. Limnol Oceanogr 45:1520–1525 CrossRefGoogle Scholar
  28. Ploug H, Stolte W, Epping EHG, Jørgensen BB (1999) Diffusive boundary layers, photosynthesis, and respiration of the colony-forming plankton algae, Phaeocystis sp. Limnol Oceanogr 44:1949–1958CrossRefGoogle Scholar
  29. Raghavendra AS, Gerst U, Heber U (1995) Oscillations in photosynthetic carbon assimilation and chlorophyll fluorescence are different in Amaranthus caudatus, a C4 plant, and Spinacia oleracea, a C3 plant. Planta 195:471–477CrossRefGoogle Scholar
  30. Raven JA (1993) Limits on growth rate. Nature 361:209–210CrossRefGoogle Scholar
  31. Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27:85–209Google Scholar
  32. Raven JA, Smith FA (1980) Intracellular pH regulation in the giant-celled marine alga Chaetomorpha darwinii. J exp Bot 31:1357–1371CrossRefGoogle Scholar
  33. Revsbech NP (1989) An oxygen microelectrode with a guard cathode. Limnol Oceanogr 34:474–478CrossRefGoogle Scholar
  34. Roberts K, Granum E, Leegood RC, Raven JA (2007a) Carbon acquisition by diatoms. Photosynth Res, DOI 10.1007.s11120-007-9172-2Google Scholar
  35. Roberts K, Granum E, Leegood RC, Raven JA (2007b) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental control. Plant Physiol 145. doi: 10.1104/pp107.10261
  36. Rovers W, Giersch C (1995) Photosynthetic oscillations and the interdependence of photophosphorylation and electron transport as studied by a mathematical model. BioSystems 35:63–73PubMedCrossRefGoogle Scholar
  37. Roussel MR (1998) Slowly reverting enzyme inactivation: a mechanism for generating long-lived damped oscillations. J theor Biol 195:233–244PubMedCrossRefGoogle Scholar
  38. Ryde-Pettersson U (1992) Oscillations in the photosynthetic Calvin cycle: examination of a mathematical model. Acta Chim Scand 46:406–408CrossRefGoogle Scholar
  39. Setlikova E, Setlik I, Kupper H, Kasilicky V, Prasil O (2005) The photosynthesis of individual algal cells during the cell cycle of Scenedesmus quadricauda studied by chlorophyll fluorescence kinetic microscopy. Photosynth Res 84:113–120 PubMedCrossRefGoogle Scholar
  40. Siebke K, Weis E (1995) Imaging of chlorophyll-a-fluorescence in leaves: topography of photosynthetic oscillations in leaves of Glechoma hederacea. Photosynth Res 45:225–237CrossRefGoogle Scholar
  41. Siebke K, Yin Z-H, Raghavendra AS, Heber U (1992) Vacuolar pH oscillations in mesophyll cells accompany oscillations of photosynthesis in leaves: interdependence of cellular compartments, and regulation of electron flow in photosynthesis. Planta 186:526–531CrossRefGoogle Scholar
  42. Sivak MN (1987) Oscillations and other symptoms of limitation of in vivo photosynthesis by inadequate phosphate supply to the chloroplast. Plant Physiol Biochem 25:635–648Google Scholar
  43. Smith FA, Raven JA (1979) Intracellular pH and its regulation. Ann Rev Plant Physiol 30:289–311CrossRefGoogle Scholar
  44. Stitt M, Grosse H (1988) Interactions between sucrose synthesis and CO2 fixation I. Secondary kinetics during photosynthesis induction are related to a delayed activation of sucrose synthesis. J Plant Physiol 133:129–137Google Scholar
  45. Stitt M, Grosse H, Woo K-C (1988) Interactions between sucrose synthesis and CO2 fixation II. Alterations of fructose 2,6-bisphosphate during photosynthetic oscillations. J Plant Physiol 133:138–143Google Scholar
  46. Taraldsvik M, Myklestad SM (2000) The effect of pH on growth rate, biochemical composition and extracellular production of the marine diatom Skeletonema costatum. Eur J Phycol 35:189–194CrossRefGoogle Scholar
  47. Underwood GJC, Perkins RG, Consalvey MC, Hanlon ARM, Oxborough K, Baker NR, Paterson DM (2005) Patterns in microphytobenthic primary productivity: species-specific variation in migratory rhythms and photosynthetic efficiency in mixed-species biofilms. Limnol Oceanogr 50:755–767CrossRefGoogle Scholar
  48. Vanselow KH, Kolbowski J, Hansen U-P (1989) Further evidence for the relationship between light-induced-changes of plasmalemma transport and transthylakoid proton uptake. J exp Bot 40:239–245CrossRefGoogle Scholar
  49. Villareal TA (2004) Single-cell pulse amplitude modulation fluorescence measurements of the giant diatom Ethmodiscus (Bacillariophyceae). J Phycol 40:1052–1061CrossRefGoogle Scholar
  50. Vredenberg WF (1969) Light-induced changes in membrane potential connected with photosynthetic electron transport. Biochem Biophys Res Comm 37:785–792PubMedCrossRefGoogle Scholar
  51. Wolf-Gladrow DA, Riebesell U, Burkhardt S, Bijma J (1999) Direct effect of CO2 concentration on growth and isotopic composition of marine plankton. Tellus—Chem Phys Meteorol 51B:461–476Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Marine Botany (FB2)University of BremenBremenGermany
  2. 2.Plant Research Unit, Scottish Crop Research InstituteUniversity of Dundee at SCRIInvergowrieUK

Personalised recommendations