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

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 growth-phase 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

Warm plankton soup and red herrings: calcareous nannoplankton cellular communities and the Palaeocene–Eocene Thermal Maximum

Past global warming events such as the Palaeocene–Eocene Thermal Maximum (PETM—56 Ma) are attributed to the release of vast amounts of carbon into the ocean, atmosphere and biosphere with recovery ascribed to a combination of silicate weathering and organic carbon burial. The phytoplanktonic nannoplankton are major contributors of organic and inorganic carbon but their role in this recovery process remains poorly understood and complicated by their contribution to marine calcification. Biocalcification is implicated not only in long-term carbon burial but also both short-term positive and negative climatic feedbacks associated with seawater buffering and responses to ocean acidification. Here, we use exceptional records of preserved fossil coccospheres to reconstruct cell size distribution, biomass production (particulate organic carbon, POC) and (particulate) inorganic carbon (PIC) yields of three contrasting nannoplankton communities (Bass River—outer shelf, Maud Rise—uppermost bathyal, Shatsky Rise—open ocean) through the PETM onset and recovery. Each of the sites shows contrasting community responses across the PETM as a function of their taxic composition and total community biomass. Our results indicate that nannoplankton PIC:POC had no role in short-term climate feedback and, as such, their importance as a source of CO2 to the environment is a red herring. It is nevertheless likely that shifts to greater numbers of smaller cells at the shelf site in particular led to greater carbon transfer efficiency, and that nannoplankton productivity and export across the shelves had a significant modulating effect on carbon sequestration during the PETM recovery

Growth rates and biometric measurements of coccolithophores (Coccolithus pelagicus, Coccolithus braarudii, Emiliania huxleyi) during experiments

Coccolithophores, a diverse group of phytoplankton, make important contributions to pelagic calcite production and export, yet the comparative biogeochemical role of species other than the ubiquitous Emiliania huxleyi is poorly understood. Here we examined the relative importance of E. huxleyi and two Coccolithus species (Coccolithus pelagicus and Coccolithus braarudii), in terms of daily calcite production, by culturing E. huxleyi and Coccolithus in parallel, and comparing growth rates and biometrically determined cellular carbon calcite quotas. Biometric measurements of Coccolithus species, and E. huxleyi cell diameters, were performed using polarised light microscopy. Scanning electron microscopy was used for all other biometric measurements of E. huxleyi

Strain-specific morphological response of the dominant calcifying phytoplankton species Emiliania huxleyi to salinity change.

The future physiology of marine phytoplankton will be impacted by a range of changes in global ocean conditions, including salinity regimes that vary spatially and on a range of short- to geological timescales. Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. Previous research has shown that the morphology of their exoskeletal calcified plates (coccoliths) responds to changing salinity in the most abundant coccolithophore species, Emiliania huxleyi. However, the extent to which these responses may be strain-specific is not well established. Here we investigated the growth response of six strains of E. huxleyi under low (ca. 25) and high (ca. 45) salinity batch culture conditions and found substantial variability in the magnitude and direction of response to salinity change across strains. Growth rates declined under low and high salinity conditions in four of the six strains but increased under both low and high salinity in strain RCC1232 and were higher under low salinity and lower under high salinity in strain PLYB11. When detailed changes in coccolith and coccosphere size were quantified in two of these strains that were isolated from contrasting salinity regimes (coastal Norwegian low salinity of ca. 30 and Mediterranean high salinity of ca. 37), the Norwegian strain showed an average 26% larger mean coccolith size at high salinities compared to low salinities. In contrast, coccolith size in the Mediterranean strain showed a smaller size trend (11% increase) but severely impeded coccolith formation in the low salinity treatment. Coccosphere size similarly increased with salinity in the Norwegian strain but this trend was not observed in the Mediterranean strain. Coccolith size changes with salinity compiled for other strains also show variability, strongly suggesting that the effect of salinity change on coccolithophore morphology is likely to be strain specific. We propose that physiological adaptation to local conditions, in particular strategies for plasticity under stress, has an important role in determining ecotype responses to salinity

Black Sea outflow response to Holocene meltwater events

During the Holocene, North American ice sheet collapse and rapid sea-level rise reconnected the Black Sea with the global ocean. Rapid meltwater releases into the North Atlantic and associated climate change arguably slowed the pace of Neolithisation across southeastern Europe, originally hypothesized as a catastrophic flooding that fueled culturally-widespread deluge myths. However, we currently lack an independent record linking the timing of meltwater events, sea-level rise and environmental change with the timing of Neolithisation in southeastern Europe. Here, we present a sea surface salinity record from the Northern Aegean Sea indicative of two meltwater events at ~8.4 and ~7.6 kiloyears that can be directly linked to rapid declines in the establishment of Neolithic sites in southeast Europe. The meltwater events point to an increased outflow of low salinity water from the Black Sea driven by rapid sea level rise >1.4 m following freshwater outbursts from Lake Agassiz and the final decay of the Laurentide ice sheet. Our results shed new light on the link between catastrophic sea-level rise and the Neolithisation of southeastern Europe, and present a historical example of how coastal populations could have been impacted by future rapid sea-level rise

Coccosphere geometry measurements from culture experiments on the coccolithophore species Calcidiscus leptoporus, Calcidiscus quadriperforatus and Helicosphaera carteri

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 growth-phase 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