Light quality induces a shift in coccosphere morphology in Scyphosphaera apsteinii.

The coccolithophore Schyphosphaera apsteinii produces distinct coccolith morphotypes and offers a unique insight into coccolith calcification, as the number of lopadoliths per cell increases under low light intensities. This study employs S. apsteinii to investigate the acclimated impact of light intensity and wavelength on cell physiology and coccosphere morphology. Our findings reveal a marked increase in lopadolith production when grown under reduced light intensity, with lower growth rates, higher chlorophyll concentration and elevated net photosynthetic rates. Reduced blue-light also caused an increase in lopadolith numbers, elevated chlorophyll concentrations and net photosynthetic rates. Conversely, such responses are less pronounced under reduced red-light. Moreover, reduced blue- and red-light treatments exhibited enhanced growth rates compared to the light-replete control, despite a reduction in light intensity. Our findings suggest that changes in light quality cause a shift in the coccosphere morphology, affecting cell physiology and potentially aiding light harvesting in S. apsteinii.

Control of crystal growth during coccolith formation by the coccolithophore Gephyrocapsa oceanica.

Coccolithophores are marine phytoplankton that produce calcite mineral scales called coccoliths. Many stages in the synthesis of these structures are still unresolved, making it difficult to accurately quantify the energetic costs involved in calcification, required to determine the response coccolith mineralization will have to rising ocean acidification and temperature created by an increase in global CO2 concentrations. To clarify this, an improved understanding of how coccolithophores control the fundamental processes of crystallization, including nucleation, growth, and morphology, is needed. Here, we study how crystal growth and morphology is controlled in the coccolithophore Gephyrocapsa oceanica by imaging coccoliths at various stages of maturity using cryo-transmission electron microscopy (cryoTEM), scanning electron microscopy (SEM) and focused ion beam SEM (FIB-SEM). We reveal that coccolith units tightly interlock with each other due to the non-vertical alignment of the two-layered tube element, causing these mineral units to extend over the adjacent crystals. In specific directions, the growth of the coccolith tube seems to be impacted by the physical constraint created by the close association of neighbouring units around the ring, influencing the overall morphology and organization of the crystals that develop. Our findings contribute to the overall understanding of how biological systems can manipulate crystallization to produce functional mineralized tissues.

Meta-analysis reveals responses of coccolithophores and diatoms to warming.

A meta-analysis was conducted to explore the effects of warming on the physiological processes of coccolithophores and diatoms by synthesizing a large number of published literatures. A total of 154 studies consisting 301 experiments were synthesized in this study. Under a projected temperature increase of 3-5 °C by IPCC AR6 at the end of this century, our results suggest that the growth and photosynthetic rate of coccolithophores were significantly enhanced by the rising temperature, while the calcification of coccolithophores was only slightly promoted. Warming also had significantly positive effects on the growth but not photosynthesis of diatoms. In comparison, the effect size of warming on the growth rate of coccolithophores was larger than that of diatoms. However, there was no significant effect of warming on either the ratio of particulate inorganic carbon to particulate organic carbon (PIC:POC) of coccolithophores or the ratio of biogenic silica to carbon (BSi:C) of diatoms. Furthermore, the results reveal latitudinal and size-specific patterns of the effect sizes of warming. For diatoms, the effects of warming on growth were more prominent in high latitudes, specifically for the Southern Hemisphere species. In addition, the effect size of warming on the small-sized diatoms was larger than that of the large-sized diatoms. For coccolithophores, the growth of the Southern Hemisphere temperate strains was significantly promoted by warming. Overall, the results based on the meta-analysis indicate that the projected warming of the end of this century will be more favor to the growth of coccolithophores than that of diatoms, thus potentially affect the competitive advantages of coccolithophores over diatoms; while the mid-to high latitude species/strains of both coccolithophores and diatoms will benefit more than their counterparts in the lower latitudes. Therefore, this study offers novel insights into predicting both the inter- and intra-group competitive advantages of diatoms and coccolithophores under the future warming climate change scenario.

Ocean Acidification Affects the Response of the Coastal Coccolithophore Pleurochrysis carterae to Irradiance.

The ecologically important marine phytoplankton group coccolithophores have a global distribution. The impacts of ocean acidification on the cosmopolitan species Emiliania huxleyi have received much attention and have been intensively studied. However, the species-specific responses of coccolithophores and how these responses will be regulated by other environmental drivers are still largely unknown. To examine the interactive effects of irradiance and ocean acidification on the physiology of the coastal coccolithophore species Pleurochrysis carterae, we carried out a semi-continuous incubation experiment under a range of irradiances (50, 200, 500, 800 µmol photons m-2 s-1) at two CO2 concentration conditions of 400 and 800 ppm. The results suggest that the saturation irradiance for the growth rate was higher at an elevated CO2 concentration. Ocean acidification weakened the particulate organic carbon (POC) production of Pleurochrysis carterae and the inhibition rate was decreased with increasing irradiance, indicating that ocean acidification may affect the tolerating capacity of photosynthesis to higher irradiance. Our results further provide new insight into the species-specific responses of coccolithophores to the projected ocean acidification under different irradiance scenarios in the changing marine environment.

Two-sided effects of the organic phosphorus phytate on a globally important marine coccolithophorid phytoplankton.

Dissolved organic phosphorus (DOP) is a potential source of aquatic eutrophication and pollution because it can potentially stimulate growth in some species and inhibit growth in other species of algae, the foundation of the marine ecosystem. Inositol hexaphosphate (also named phytic acid or PA), an abundant organophosphate, is presumably ubiquitous in the marine environment, but how it affects marine primary producers is poorly understood. Here, we investigated the bioavailability of this DOP to the cosmopolitan coccolithophore Emiliania huxleyi. Our results showed that E. huxleyi cells can take up PA and dissolved inorganic phosphorus (DIP) simultaneously. Absorbed PA can efficiently support algal growth, producing cell yield between DIP and phosphorus (P)-depleted conditions. Accordingly, PA supply as the sole P source highly influences cellular metabolism and nutrient stoichiometry. Particularly, PA-grown cultures exhibited enhanced carbon fixation, increased lipid content, activated energy metabolism, and induced nitrogen assimilation. However, our data suggest that PA may also exert some levels of toxic effects on E. huxleyi. This study provides novel insights into the variable effects of a DOP on marine phytoplankton, which will inform new inquiries about how the complex DOP constituencies in the ocean will shape phytoplankton community structure and function. IMPORTANCE The dissolved organic phosphorus (DOP) utilization in phytoplankton plays vital roles in cellular P homeostasis, P-nutrient niche, and the dynamics of community structure in marine ecosystems, but its mechanisms, potentially varying with species, are far from clear. In this study, we investigated the utilization of a widespread DOP species, which is commonly produced by plants (land plants and marine macrophytes) and released into coastal areas, in a globally distributed bloom-forming coccolithophore species in various phosphorus environments. Using a combination of physiological and transcriptomic measurements and analyses, our experimental results revealed the complex mechanism and two-sided effects of DOP (major algal growth-supporting and minor toxic effects) in this species, providing a novel perspective on phytoplankton nutrient regulation.

Phylogeny and genetic variations of the three genome compartments in haptophytes shed light on the rapid evolution of coccolithophores.

Haptophyte algae, including coccolithophores, play key roles in global carbon cycling and ecosystem. They exhibit exceptional morphological and functional diversity. However, their phylogeny is mostly based on short markers and genome researches are always limited to few species, hindering a better understanding about their evolution and diversification. In this study, by assembling 69 new plastid genomes, 65 new mitochondrial genomes, and 55 nuclear drafts, we systematically analyzed their genome variations and built the most comprehensive phylogenies in haptophytes and Noelaerhabdaceae, with the latter is the family of the model coccolithophore Emiliania huxleyi. The haptophyte genomes vary significantly in size, gene content, and structure. We detected phylogenetic incongruence of Prymnesiales between genome compartments. In Noelaerhabdaceae, by including Reticulofenestra sessilis and a proper outgroup, we found R. sessilis was not the basal taxon of this family. Noelaerhabdaceae strains have very similar genomic features and conserved sequences, but different gene content and dynamic structure. We speculate that was caused by DNA double-strand break repairs. Our results provide valuable genetic resources and new insights into the evolution of haptophytes, especially coccolithophores.

Voltage-Gated Proton Channels in the Tree of Life.

With a single gene encoding HV1 channel, proton channel diversity is particularly low in mammals compared to other members of the superfamily of voltage-gated ion channels. Nonetheless, mammalian HV1 channels are expressed in many different tissues and cell types where they exert various functions. In the first part of this review, we regard novel aspects of the functional expression of HV1 channels in mammals by differentially comparing their involvement in (1) close conjunction with the NADPH oxidase complex responsible for the respiratory burst of phagocytes, and (2) in respiratory burst independent functions such as pH homeostasis or acid extrusion. In the second part, we dissect expression of HV channels within the eukaryotic tree of life, revealing the immense diversity of the channel in other phylae, such as mollusks or dinoflagellates, where several genes encoding HV channels can be found within a single species. In the last part, a comprehensive overview of the biophysical properties of a set of twenty different HV channels characterized electrophysiologically, from Mammalia to unicellular protists, is given.

Lipids of different phytoplankton groups differ in sensitivity to degradation: Implications for carbon export.

The future of life on Earth depends on how the ocean might change, as it plays an important role in mitigating the effects of global warming. The main role is played by phytoplankton. Not only are phytoplankton the base of the oceans' food web, but they also play an important role in the biological carbon pump (BCP), the process of forming organic matter (OM) and transporting it to the deep sea, representing a sink of atmospheric CO2 . Lipids are considered important vectors for carbon sequestration. A change in the phytoplankton community composition as a result of ocean warming is expected to affect the BCP. Many predictions indicate a dominance of small at the expense of large phytoplankton. To gain insight into interplay between the phytoplankton community structure, lipid production and degradation, and adverse environmental conditions, we analyzed phytoplankton composition, particulate organic carbon (POC) and its lipid fraction in the northern Adriatic over a period from winter to summer at seven stations with a gradient of trophic conditions. We found that at high salinity and low nutrient content, where nanophytoplankton prevailed over diatoms, the newly fixed carbon is substantially directed toward the synthesis of lipids. Lipids produced by nanophytoplankton, coccolithophores, and phytoflagellates, are more resistant to degradation than those produced by diatoms. The difference in lipid degradability is discussed as a difference in the size of the cell phycosphere. We hypothesize that the lipids of nanophytoplankton are less degradable due to the small phycosphere with a poorer bacterial community and consequently a lower lipid degradation rate compared with diatoms. The lipid chemical composition of the different phytoplankton groups could have a different susceptibility to degradation. Results suggest a successful lipid carbon sink of nanophytoplankton and, thus, a negative feedback on global warming.

Interaction matters: Bottom-up driver interdependencies alter the projected response of phytoplankton communities to climate change.

Phytoplankton growth is controlled by multiple environmental drivers, which are all modified by climate change. While numerous experimental studies identify interactive effects between drivers, large-scale ocean biogeochemistry models mostly account for growth responses to each driver separately and leave the results of these experimental multiple-driver studies largely unused. Here, we amend phytoplankton growth functions in a biogeochemical model by dual-driver interactions (CO2 and temperature, CO2 and light), based on data of a published meta-analysis on multiple-driver laboratory experiments. The effect of this parametrization on phytoplankton biomass and community composition is tested using present-day and future high-emission (SSP5-8.5) climate forcing. While the projected decrease in future total global phytoplankton biomass in simulations with driver interactions is similar to that in control simulations without driver interactions (5%-6%), interactive driver effects are group-specific. Globally, diatom biomass decreases more with interactive effects compared with the control simulation (-8.1% with interactions vs. no change without interactions). Small-phytoplankton biomass, by contrast, decreases less with on-going climate change when the model accounts for driver interactions (-5.0% vs. -9.0%). The response of global coccolithophore biomass to future climate conditions is even reversed when interactions are considered (+33.2% instead of -10.8%). Regionally, the largest difference in the future phytoplankton community composition between the simulations with and without driver interactions is detected in the Southern Ocean, where diatom biomass decreases (-7.5%) instead of increases (+14.5%), raising the share of small phytoplankton and coccolithophores of total phytoplankton biomass. Hence, interactive effects impact the phytoplankton community structure and related biogeochemical fluxes in a future ocean. Our approach is a first step to integrate the mechanistic understanding of interacting driver effects on phytoplankton growth gained by numerous laboratory experiments into a global ocean biogeochemistry model, aiming toward more realistic future projections of phytoplankton biomass and community composition.

High-CO2 Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance.

The coccolithophore Emiliania huxleyi shows a variety of responses to ocean acidification (OA) and to high-CO2 concentrations, but there is still controversy on differentiating between these two factors when using different strains and culture methods. A heavily calcified type A strain isolated from the Norwegian Sea was selected and batch cultured in order to understand whether acclimation to OA was mediated mainly by CO2 or H+, and how it impacted cell growth performance, calcification, and physiological stress management. Emiliania huxleyi responded differently to each acidification method. CO2-enriched aeration (1200 µatm, pH 7.62) induced a negative effect on the cells when compared to acidification caused by decreasing pH alone (pH 7.60). The growth rates of the coccolithophore were more negatively affected by high pCO2 than by low pH without CO2 enrichment with respect to the control (400 µatm, pH 8.1). High CO2 also affected cell viability and promoted the accumulation of reactive oxygen species (ROS), which was not observed under low pH. This suggests a possible metabolic imbalance induced by high CO2 alone. In contrast, the affinity for carbon uptake was negatively affected by both low pH and high CO2. Photochemistry was only marginally affected by either acidification method when analysed by PAM fluorometry. The POC and PIC cellular quotas and the PIC:POC ratio shifted along the different phases of the cultures; consequently, calcification did not follow the same pattern observed in cell stress and growth performance. Specifically, acidification by HCl addition caused a higher proportion of severely deformed coccoliths, than CO2 enrichment. These results highlight the capacity of CO2 rather than acidification itself to generate metabolic stress, not reducing calcification.

Emiliania huxleyi-Bacteria Interactions under Increasing CO2 Concentrations.

The interactions established between marine microbes, namely phytoplankton-bacteria, are key to the balance of organic matter export to depth and recycling in the surface ocean. Still, their role in the response of phytoplankton to rising CO2 concentrations is poorly understood. Here, we show that the response of the cosmopolitan Emiliania huxleyi (E. huxleyi) to increasing CO2 is affected by the coexistence with bacteria. Specifically, decreased growth rate of E. huxleyi at enhanced CO2 concentrations was amplified in the bloom phase (potentially also related to nutrient concentrations) and with the coexistence with Idiomarina abyssalis (I. abyssalis) and Brachybacterium sp. In addition, enhanced CO2 concentrations also affected E. huxleyi's cellular content estimates, increasing organic and decreasing inorganic carbon, in the presence of I. abyssalis, but not Brachybacterium sp. At the same time, the bacterial isolates only survived in coexistence with E. huxleyi, but exclusively I. abyssalis at present CO2 concentrations. Bacterial species or group-specific responses to the projected CO2 rise, together with the concomitant effect on E. huxleyi, might impact the balance between the microbial loop and the export of organic matter, with consequences for atmospheric carbon dioxide.

Novel combination coccospheres from Helicosphaera spp indicate complex relationships between species.

Coccolithophores play an important role in global biogeochemical cycling, but many aspects of their ecology remain poorly understood, including their heteromorphic haplo-diplontic life cycle. The presence of combination coccospheres in environmental samples, which represent a transition between the lightly calcified haploid (HOL) and heavily calcified diploid (HET) life phases, provides crucial evidence linking the two life cycle phases of a particular species. Here, we describe combination coccospheres from the Southern Ocean that show a novel association between Helicosphaera hyalina (HET) and Helicosphaera HOL catilliferus type. The ability of Helicosphaera HET and HOL morphospecies to form multiple different combinations indicates a substantial complexity in the relationships between life cycle phases in this group. The findings suggest recent divergence within the Helicosphaera lineage may have resulted in significant inter- and intra-specific variability, with cryptic speciation in one or both life cycle phases contributing to their ability to form multiple HET/HOL associations.

Variation in biogenic calcite production by coccolithophores across mesoscale eddies in the Bay of Bengal.

Coccolithophore calcite production (CP) was investigated for the first time in the Bay of Bengal. Against expectation, calcite production was not fueled by the nutrient-enriched cold eddy because of the reduced light penetration. CP rate was observed to be higher at the anticyclonic eddy possibly benefited from rare species production. The adjoining river-induced shallow mixed-layer depth and eddy activity co-influenced CP rate. On average, the integrated CP rates were 0.04, 0.15, and 0.07 mmol C m-2 h-1 for the cyclonic eddy, anticyclonic eddy, and outer area, respectively. In the upper photic waters, CP rates showed a strong correlation with primary productivity (PP). However, a decoupling of CP and PP was observed in the lower photic zone due to differential light and nitrogen preferences in calcification and carbon fixation. Our findings could help to understand the biogenic response of eddy and inorganic-organic carbon association in the pelagic biogeochemical cycles.

Allometry of carbon and nitrogen content and growth rate in a diverse range of coccolithophores.

As both photoautotrophs and calcifiers, coccolithophores play important roles in ecosystems and biogeochemical cycles. Though some species form blooms in high-latitude waters, low-latitude communities exhibit high diversity and niche diversification. Despite such diversity, our understanding of the clade relies on knowledge of Emiliana huxleyi. To address this, we examine carbon (C) and nitrogen (N) content of strains (n = 9) from the main families of the calcifying Haptophyceae, as well as allometry and cell size frequency across extant species. Coccolithophore cell size is constrained, with ~71% of 159 species smaller than 10 µm in diameter. Growth rates scale with cell biovolume (µ = 1.83 × cell volume-0.19), with an exponent close to metabolic theory. Organic carbon (C) per cell is lower than for other phytoplankton, providing a coccolithophore-specific relationship between cell organic C content and biovolume (pg C cell-1 = 0.30 × cell volume0.70). Organic C to N ratios (~8.3 mol:mol) are similar to other phytoplankton, implying little additional N cost for calcification and efficient retention and recycling of cell N. Our results support observations that coccolithophores are efficient competitors in low-nutrient conditions, able to photosynthesize, calcify and run the routine metabolic machinery necessary without any additional need for N relative to noncalcifying algae.

Coccolith crystals: Pure calcite or organic-mineral composite structures?

The localization of organic material within biominerals is central to developing biomineral formation mechanisms. Coccoliths, morphologically sophisticated calcite platelets of intracellularly calcifying coccolithophores, are not only eco-physiologically important, but also influence biogeochemical cycles through mass production. Despite their importance and over a century of research, the formation mechanism of coccoliths is still poorly understood. Crucial unsolved questions include the localization of organic material within coccoliths. In extracellular calcifiers the discovery of an organics-containing nano-structure within seemingly single crystals has led to the formulation of a two-step crystallization mechanism. Coccoliths are traditionally thought of as being formed by a different mechanism, but it is unclear whether coccolith crystals possess a nano-structure. Here we review the evidence for and against such a nano-structure. Current SXPD analyses suggest a nano-structure of some kind, while imaging methods (SEM, TEM, AFM) provide evidence against it. We suggest directions for future research which should help solve this puzzle. STATEMENT OF SIGNIFICANCE: Coccolithophores, unicellular calcifying algae, are important primary producers and contribute significantly to pelagic calcium carbonate export. Their calcite platelets, the coccoliths, are amongst the most sophisticated biomineral structures. Understanding the crystallization mechanism of coccolith crystals is not only central to coccolithophore cell biology but also lies at the heart of biomineralization research more generally. The crystallization mechanism of coccoliths has remained largely elusive, not least because it is still an open question whether the micron sized coccolith crystals are pure calcite, or contain organic material. Here we review the state of the art and suggest a way to solve this central problem.

Genome Sequence of Chrysotila roscoffensis, a Coccolithphore Contributed to Global Biogeochemical Cycles.

Chrysotila is a genus of coccolithophores. Together with Emiliania, it is one of the representative genera in the Haptophyta which have been extensively studied. They are photosynthetic unicellular marine algae sharing the common characteristic of the production of CaCO3 platelets (coccoliths) on the surface of their cells and are crucial contributors to global biogeochemical cycles. Here, we report the genome assembly of Chrysotila roscoffensis. The assembled genome size was ~636 Mb distributed across 769 scaffolds with N50 of 1.63 Mb, and maximum contig length of ~2.6 Mb. Repetitive elements accounted for approximately 59% of the genome. A total of 23,341 genes were predicted from C. roscoffensis genome. The divergence time between C. roscoffensis and Emiliania huxleyi was estimated to be around 537.6 Mya. Gene families related to cytoskeleton, cellular motility and morphology, and ion transport were expanded. The genome of C. roscoffensis will provide a foundation for understanding the genetic and phenotypic diversification and calcification mechanisms of coccolithophores.

Detection of Coccolithophore Blooms With BioGeoChemical-Argo Floats.

Coccolithophores (calcifying phytoplankton) form extensive blooms in temperate and subpolar oceans as evidenced from ocean-color satellites. This study examines the potential to detect coccolithophore blooms with BioGeoChemical-Argo (BGC-Argo) floats, autonomous ocean profilers equipped with bio-optical and physicochemical sensors. We first matched float data to ocean-color satellite data of calcite concentration to select floats that sampled coccolithophore blooms. We identified two floats in the Southern Ocean, which measured the particulate beam attenuation coefficient (c p) in addition to two core BGC-Argo variables, Chlorophyll-a concentration ([Chl-a]) and the particle backscattering coefficient (b bp). We show that coccolithophore blooms can be identified from floats by distinctively high values of (1) the b bp/c p ratio, a proxy for the refractive index of suspended particles, and (2) the b bp/[Chl-a] ratio, measurable by any BGC-Argo float. The latter thus paves the way to global investigations of environmental control of coccolithophore blooms and their role in carbon export.

Dataset of theEmiliania huxleyi abundance and phytoplankton composition in the Barents Sea in 2014-2018.

This data article contains data on the Emiliania huxleyi abundance, phytoplankton composition, in the Barents Sea in summer 2014-2018, and physical and hydrochemical parameters in summer 2017. The data are based on the samples collected on stations, where E. huxleyi blooms were recorded. The physical data included the water temperature, salinity, oxygen concentrations at the surface, and various depths. Data of nutrients concentrations included followed parameters: silicates, phosphates, nitrates, nitrites, ammonium, and dissolved inorganic nitrogen. The nutrients ratios are also given. Data of phytoplankton composition consists of the abundance of diatoms, dinoflagellates, coccolithophores, and small flagellates. The data presented in this article are associated with the research article entitled "Interannual variability of Emiliania huxlei blooms in the Barents Sea: In Situ data 2014-2018" [1]. The related research article examines the influence of abiotic factors such as temperature, salinity, nutrients concentrations, and biotic factors (phytoplankton composition) on E. huxleyi abundance.

Effects of multiple drivers of ocean global change on the physiology and functional gene expression of the coccolithophore Emiliania huxleyi.

Ongoing ocean global change due to anthropogenic activities is causing multiple chemical and physical seawater properties to change simultaneously, which may affect the physiology of marine phytoplankton. The coccolithophore Emiliania huxleyi is a model species often employed in the study of the marine carbon cycle. The effect of ocean acidification (OA) on coccolithophore calcification has been extensively studied; however, physiological responses to multiple environmental drivers are still largely unknown. Here we examined two-way and multiple driver effects of OA and other key environmental drivers-nitrate, phosphate, irradiance, and temperature-on the growth, photosynthetic, and calcification rates, and the elemental composition of E. huxleyi. In addition, changes in functional gene expression were examined to understand the molecular mechanisms underpinning the physiological responses. The single driver manipulation experiments suggest decreased nitrate supply being the most important driver regulating E. huxleyi physiology, by significantly reducing the growth, photosynthetic, and calcification rates. In addition, the interaction of OA and decreased nitrate supply (projected for year 2100) had more negative synergistic effects on E. huxleyi physiology than all other two-way factorial manipulations, suggesting a linkage between the single dominant driver (nitrate) effects and interactive effects with other drivers. Simultaneous manipulation of all five environmental drivers to the conditions of the projected year 2100 had the largest negative effects on most of the physiological metrics. Furthermore, functional genes associated with inorganic carbon acquisition (RubisCO, AEL1, and δCA) and calcification (CAX3, AEL1, PATP, and NhaA2) were most downregulated by the multiple driver manipulation, revealing linkages between responses of functional gene expression and associated physiological metrics. These findings together indicate that for more holistic projections of coccolithophore responses to future ocean global change, it is necessary to understand the relative importance of environmental drivers both individually (i.e., mechanistic understanding) and interactively (i.e., cumulative effect) on coccolithophore physiology.