Articles | Volume 12, issue 21
Biogeosciences, 12, 6493–6501, 2015
Biogeosciences, 12, 6493–6501, 2015

Research article 13 Nov 2015

Research article | 13 Nov 2015

Phytoplankton calcification as an effective mechanism to alleviate cellular calcium poisoning

M. N. Müller1,2, J. Barcelos e Ramos3, K. G. Schulz4, U. Riebesell5, J. Kaźmierczak6, F. Gallo3, L. Mackinder7, Y. Li8, P. N. Nesterenko8, T. W. Trull9, and G. M. Hallegraeff1 M. N. Müller et al.
  • 1Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Private Bag 129, Hobart, TAS 7001, Australia
  • 2Institute of Oceanography, University of São Paulo, Praça do Oceanográfico 191, 05508-120 São Paulo, SP, Brazil
  • 3Centre of Climate, Meteorology and Global Change (CMMG), University of Azores, Rua do Capitão d'Ávila, Pico da Urze 970-0042 Angra do Heroísmo, Açores, Portugal
  • 4Centre for Coastal Biogeochemistry, School of Environmental Science and Management, Southern Cross University, P.O. Box 157, Lismore, NSW 2480, Australia
  • 5GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105 Kiel, Germany
  • 6Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warsaw, Poland
  • 7Department of Plant Biology, Carnegie Institution, 260 Panama Street, Stanford, CA 94305, USA
  • 8Australian Centre for Research on Separation Science (ACROSS), School of Chemistry, University of Tasmania, Private Bag 75, Hobart, TAS 7001, Australia
  • 9Antarctic Climate and Ecosystems Cooperative Research Centre, University of Tasmania and CSIRO Oceans and Atmosphere Flagship, Hobart, TAS 7001, Australia

Abstract. Marine phytoplankton have developed the remarkable ability to tightly regulate the concentration of free calcium ions in the intracellular cytosol at a level of ~ 0.1 μmol L−1 in the presence of seawater Ca2+ concentrations of 10 mmol L−1. The low cytosolic calcium ion concentration is of utmost importance for proper cell signalling function. While the regulatory mechanisms responsible for the tight control of intracellular Ca2+ concentration are not completely understood, phytoplankton taxonomic groups appear to have evolved different strategies, which may affect their ability to cope with changes in seawater Ca2+ concentrations in their environment on geological timescales. For example, the Cretaceous (145 to 66 Ma), an era known for the high abundance of coccolithophores and the production of enormous calcium carbonate deposits, exhibited seawater calcium concentrations up to 4 times present-day levels. We show that calcifying coccolithophore species (Emiliania huxleyi, Gephyrocapsa oceanica and Coccolithus braarudii) are able to maintain their relative fitness (in terms of growth rate and photosynthesis) at simulated Cretaceous seawater calcium concentrations, whereas these rates are severely reduced under these conditions in some non-calcareous phytoplankton species (Chaetoceros sp., Ceratoneis closterium and Heterosigma akashiwo). Most notably, this also applies to a non-calcifying strain of E. huxleyi which displays a calcium sensitivity similar to the non-calcareous species. We hypothesize that the process of calcification in coccolithophores provides an efficient mechanism to alleviate cellular calcium poisoning and thereby offered a potential key evolutionary advantage, responsible for the proliferation of coccolithophores during times of high seawater calcium concentrations. The exact function of calcification and the reason behind the highly ornate physical structures of coccoliths remain elusive.

Short summary
The White Cliffs of Dover date back to the Cretaceous and are made up of microscopic chalky shells which were produced mainly by marine phytoplankton (coccolithophores). This is iconic proof for their success at times of relatively high seawater calcium concentrations and, as shown here, to be linked to their ability to precipitate calcium as chalk. The invention of calcification can thus be considered an evolutionary milestone allowing coccolithophores to thrive at times when others struggled.
Final-revised paper