ReviewMARINE BIOLOGY

Why marine phytoplankton calcify

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Science Advances  13 Jul 2016:
Vol. 2, no. 7, e1501822
DOI: 10.1126/sciadv.1501822
  • Fig. 1 Evolutionary history of coccolithophores.

    (A) Coccolithophore species richness over time [combining heterococcoliths and nannoliths; data from Bown et al. (10)]. Q, Quaternary; N, Neogene; Pal, Paleogene; E/O, Eocene/Oligocene glacial onset event; PETM, Paleocene/Eocene thermal maximum warming event; K/Pg, Cretaceous/Paleogene; OAE, oceanic anoxic event; T-OAE, Toarcian oceanic anoxic event; T/J, Triassic/Jurassic; P/T, Permian/Triassic; mass ext., mass extinction. (B) The fossil record of major coccolithophore biomineralization innovations and morphogroups, including the first appearances of muroliths (simple coccoliths with narrow, wall-like rims), placoliths (coccoliths with broad shields that interlock to form strong coccospheres), holococcoliths (coccoliths formed from microcrystals in the haploid life cycle phase), Braarudosphaera (pentagonal, laminated nannoliths forming dodecahedral coccospheres); Calciosolenia (distinct, rhombic murolith coccoliths), Coccolithus (long-ranging and abundant Cenozoic genus), Isochrysidales (dominant order that includes Emiliania, Gephyrocapsa, and Reticulofenestra). Significant mass extinctions and paleoceanographic/paleoclimatic events are marked as horizontal lines.

  • Fig. 2 Schematic of the cellular processes associated with calcification and the approximate energetic costs of a coccolithophore cell.

    Energetic costs are reported in percentage of total photosynthetic budget. (A) Transport processes include the transport into the cell from the surrounding seawater of primary calcification substrates Ca2+ and HCO3 (black arrows) and the removal of the end product H+ from the cell (gray arrow). The transport of Ca2+ through the cytoplasm to the CV is the dominant cost associated with calcification (Table 1). (B) Metabolic processes include the synthesis of CAPs (gray rectangles) by the Golgi complex (white rectangles) that regulate the nucleation and geometry of CaCO3 crystals. The completed coccolith (gray plate) is a complex structure of intricately arranged CAPs and CaCO3 crystals. (C) Mechanical and structural processes account for the secretion of the completed coccoliths that are transported from their original position adjacent to the nucleus to the cell periphery, where they are transferred to the surface of the cell. The costs associated with these processes are likely to be comparable to organic-scale exocytosis in noncalcifying haptophyte algae.

  • Plate 1 Diversity of coccolithophores.

    Emiliania huxleyi, the reference species for coccolithophore studies, is contrasted with a range of other species spanning the biodiversity of modern coccolithophores. All images are scanning electron micrographs of cells collected by seawater filtration from the open ocean. (A to N) Species illustrated: (A) Coccolithus pelagicus, (B) Calcidiscus leptoporus, (C) Braarudosphaera bigelowii, (D) Gephyrocapsa oceanica, (E) E. huxleyi, (F) Discosphaera tubifera, (G) Rhabdosphaera clavigera, (H) Calciosolenia murrayi, (I) Umbellosphaera irregularis, (J) Gladiolithus flabellatus, (K and L) Florisphaera profunda, (M) Syracosphaera pulchra, and (N) Helicosphaera carteri. Scale bar, 5 μm.

  • Fig. 3 Proposed main benefits of calcification in coccolithophores.

    (A) Accelerated photosynthesis includes CCM (1) and enhanced light uptake via scattering of scarce photons for deep-dwelling species (2). (B) Protection from photodamage includes sunshade protection from ultraviolet (UV) light and photosynthetic active radiation (PAR) (1) and energy dissipation under high-light conditions (2). (C) Armor protection includes protection against viral/bacterial infections (1) and grazing by selective (2) and nonselective (3) grazers.

  • Fig. 4 Potential niches of calcification benefits in coccolithophores using the MITgcm model.

    Model results show the geographical area of four tested benefits of calcification. (A) Benefit of light uptake (captured by increased photosynthesis-curve slope of the coccolithophore type). (B) Benefit of high-light protection (captured by reduced light inhibition of the coccolithophore type). (C) Benefit of protection against viral/bacterial infection (captured by reduced mortality rate of the coccolithophore type). (D) Benefit of grazing protection (captured in the model by reduced palatability of the coccolithophore type). Presented model results are from the most realistic simulations when compared with biomass observations along the AMT (fig. S3).

  • Table 1 Percentage of the total photosynthetic energy budget dedicated to components of calcification.

    The budget is presented for two main coccolithophore species (E. huxleyi and C. pelagicus). PIC, particulate inorganic carbon.

    ProcessE. huxleyiC. pelagicus
    Ca2+ transport3% (CV pH of 8) to 20% (CV pH of 7.5)*≫20%
    HCO3 transport5%Undocumented but expected to be significant to sustain high PIC production rate
    H+ (removal) transport<5%§5%*
    Polysaccharide generation7%0.2%
    Total20–37%≫25%

    *Measured by Anning et al. (30).

    †Estimated from E. huxleyi, assuming a 10-fold higher PIC production rate.

    ‡Because there is no direct measurement of HCO3 accumulation in the cytoplasm, we used measurement of total cellular dissolved inorganic carbon (DIC) by Sekino and Shiraiwa (31), which is equivalent to a 10-fold accumulation. Following the electrochemical potential gradient equation for HCO3, ΔμHCO3 = RTlnCo/Ci + zFV (in kilojoules per mole), where Δμ is the electrochemical potential gradient, R is the gas constant, F is the Faraday constant, z is the valency, T is the temperature, Co and Ci are the external and internal concentrations of HCO3, and V is the membrane potential (measured at −50 mV); a 10-fold HCO3 concentration gradient across the membrane corresponds to ΔμHCO3 ~ 10 kJ/mol. Considering that 1 mol of adenosine triphosphate (ATP) provides ~ 50 kJ per mole of energy for transport, moving 1 mol of HCO3 against its electrochemical potential gradient then requires 0.2 ATP. Assuming a requirement of 3.2 ATP per mole for CO2 fixation and that 1 mol of transported HCO3 produces 1 mol of CO32− and a 1:1 calcification/photosynthesis ratio, the cost of HCO3 transport in terms of ATP required to fix 1 mol of CO2 by photosynthesis is thus equal to 0.2/3.2 ~ 5%.

    §Estimated from C. pelagicus, assuming a lower PIC production rate, resulting in lower generation of H+.

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/2/7/e1501822/DC1

      Supplementary Text

      table S1. Definition of the scores for the model-data comparison.

      fig. S1. Latitudinal biomass of two main coccolithophore types along the AMT.

      fig. S2. Testing of hypothetical costs and benefits of coccolithophore calcification in a global ocean ecological model.

      fig. S3. Assessment against observations of modeled coccolithophore distribution for the four tested benefits of calcification.

      fig. S4. Observed relationship between sinking velocity, PIC/POC ratio, coccosphere size, and cell density of E. huxleyi (black circles) and G. oceanica cultured at 15°C (blue squares) and 20°C (red triangles).

    • Supplementary Materials

      This PDF file includes:

      • Supplementary Text
      • table S1. Definition of the scores for the model-data comparison.
      • fig. S1. Latitudinal biomass of two main coccolithophore types along the AMT.
      • fig. S2. Testing of hypothetical costs and benefits of coccolithophore calcification in a global ocean ecological model.
      • fig. S3. Assessment against observations of modeled coccolithophore distribution for the four tested benefits of calcification.
      • fig. S4. Observed relationship between sinking velocity, PIC/POC ratio, coccosphere size, and cell density of E. huxleyi (black circles) and G. oceanica cultured at 15°C (blue squares) and 20°C (red triangles).

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