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Review
.2016 Jul 13;2(7):e1501822.
doi: 10.1126/sciadv.1501822. eCollection 2016 Jul.

Why marine phytoplankton calcify

Affiliations
Review

Why marine phytoplankton calcify

Fanny M Monteiro et al. Sci Adv..

Abstract

Calcifying marine phytoplankton-coccolithophores- are some of the most successful yet enigmatic organisms in the ocean and are at risk from global change. To better understand how they will be affected, we need to know "why" coccolithophores calcify. We review coccolithophorid evolutionary history and cell biology as well as insights from recent experiments to provide a critical assessment of the costs and benefits of calcification. We conclude that calcification has high energy demands and that coccolithophores might have calcified initially to reduce grazing pressure but that additional benefits such as protection from photodamage and viral/bacterial attack further explain their high diversity and broad spectrum ecology. The cost-benefit aspect of these traits is illustrated by novel ecosystem modeling, although conclusive observations remain limited. In the future ocean, the trade-off between changing ecological and physiological costs of calcification and their benefits will ultimately decide how this important group is affected by ocean acidification and global warming.

Keywords: Coccolithophores; calcification; ecological and physiological costs and benefits; ecosystem modeling; photosynthesis; trade-offs.

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Figures

Fig. 1
Fig. 1. Evolutionary history of coccolithophores.
(A) Coccolithophore species richness over time [combining heterococcoliths and nannoliths; data from Bownet 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 includesEmiliania,Gephyrocapsa, andReticulofenestra). Significant mass extinctions and paleoceanographic/paleoclimatic events are marked as horizontal lines.
Fig. 2
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
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 toN) 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
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
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).
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References

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