Physiology regulates the relationship between coccosphere geometry and growth phase in coccolithophores

Abstract

Abstract. Coccolithophores are an abundant phytoplankton group that exhibit remarkable diversity in their biology, ecology and calcitic exoskeletons (coccospheres). Their extensive fossil record is a testament to their important biogeochemical role and is a valuable archive of biotic responses to environmental change stretching back over 200 million years. However, to realise the full potential of this archive for (palaeo-)biology and biogeochemistry requires an understanding of the physiological processes that underpin coccosphere architecture. Using culturing experiments on four modern coccolithophore species (Calcidiscus leptoporus, Calcidiscus quadriperforatus, Helicosphaera carteri and Coccolithus braarudii) from three long-lived families, we investigate how coccosphere architecture responds to shifts from exponential (rapid cell division) to stationary (slowed cell division) growth phases as cell physiology reacts to nutrient depletion. These experiments reveal statistical differences in coccosphere size and the number of coccoliths per cell between these two growth phases, specifically that cells in exponential-phase growth are typically smaller with fewer coccoliths, whereas cells experiencing growth-limiting nutrient depletion have larger coccosphere sizes and greater numbers of coccoliths per cell. Although the exact numbers are species-specific, these growth-phase shifts in coccosphere geometry demonstrate that the core physiological responses of cells to nutrient depletion result in increased coccosphere sizes and coccoliths per cell across four different coccolithophore families (Calcidiscaceae, Coccolithaceae, Isochrysidaceae and Helicosphaeraceae), a representative diversity of this phytoplankton group. Building on this, the direct comparison of coccosphere geometries in modern and fossil coccolithophores enables a proxy for growth phase to be developed that can be used to investigate growth responses to environmental change throughout their long evolutionary history. Our data also show that changes in growth rate and coccoliths per cell associated with growthphase shifts can substantially alter cellular calcite production. Coccosphere geometry is therefore a valuable tool for accessing growth information in the fossil record, providing unprecedented insights into the response of species to environmental change and the potential biogeochemical consequences.

Phosphorus limitation and heat stress decrease calcification in <i>Emiliania huxleyi</i>

“…Cell concentrations, residual phosphate, A T , pH, DIC and Ca in the culture media at the time of harvest of semi-continuous and batch control and P-limited cultures of Emiliania huxleyi grown at 19 and 24 • C; n = 3 ± standard deviation. this study has been previously described by others for E. huxleyi (Paasche and Brubak, 1994;Riegman et al, 2000;Müller et al, 2008;Gibbs et al, 2013;Oviedo et al, 2014) and recently also for other species, such as C. pelagicus, Helicosphaera carteri and two Calcidiscus species Sheward et al, 2017) and may thus be a common feature of coccolithophores. Cells that are arrested in the G1 (assimilation) phase of the cell cycle (Gibbs et al, 2013) accumulate not only POC but also PIC, leading to the 2-3-fold increase in coccolith number per cell observed in stationary phase cultures (Fig.…”

“…P starvation blocks the synthesis of DNA and membrane phospholipids, necessary for cell replication, arresting the cells in the G1 (assimilation) phase of the cell cycle (Müller et al, 2008). The assimilation phase is thus prolonged and the cell continues assimilating POC, presumably in the form of non-essential lipids and carbohydrates (Sheward et al, 2017), leading to an increase in cell size (Aloisi, 2015). A similar increase in cell size to the one observed in Table 5.…”

Peer Review #3 of "Coccolith arrangement follows Eulerian mathematics in the coccolithophore Emiliania huxleyi (v0.1)"

“…This conclusion is consistent with previous studies that have observed that other coccolithophore species, Helicosphaera carteri, Toweius pertusus, and Umbilicosphaera bramletti, have minimum numbers (five to seven) of coccoliths per cell (Gibbs et al 2013;Sheward 2016;Sheward et al 2017;Young et al 2017).…”

“…This study found that larger coccospheres of E. huxleyi used more coccoliths to cover their larger surface area (p < 0.0001, Fig. 8), which was consistent with several recent studies (Gibbs et al 2013;Hoffmann et al 2015;Sheward 2016;Sheward et al 2017). Cell size is tightly regulated during the whole cell cycle to maintain the characteristic cell size of a population (Amodeo & Skotheim 2016;Kiyomitsu 2015).…”

Insensitivity of alkenone carbon isotopes to atmospheric CO&lt;sub&gt;2&lt;/sub&gt; at low to moderate CO&lt;sub&gt;2&lt;/sub&gt; levels

“…(Bidigare et al, 1997), and planktic foraminiferal δ 11 B values (CO 2(δ 11 Bplank) ), based on the pH control of boron speciation and isotopic fractionation in seawater (Hemming and Hanson, 1992). Multiple records of atmospheric pCO 2 now exist for the Cenozoic from both methods, showing a broadly similar long-term trend from a high-CO 2 greenhouse world of the early Cenozoic, when CO 2 exceeded 400 µatm and may have been higher than 1000 µatm, to a low-CO 2 bipolar glaciated world of the Late Pleistocene, when CO 2 fell to below 300 µatm (Pagani et al, 2005(Pagani et al, , 2011Pearson et al, 2009;Anagnostou et al, 2016;Foster et al, 2017;Sosdian et al, 2018;Super et al, 2018).…”