Biocalcification in porcelaneous foraminifera.

Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ 'mineralization of extracellular matrix' attributed to hyaline rotaliid shells, or 'mineralization within intracellular vesicles' attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We have found under a high-resolution scanning electron microscopy (SEM) that precipitation of high-Mg calcitic mesocrystals in porcelaneous shells takes place in situ and form a dense, chaotic meshwork of needle-like crystallites. We have not observed calcified needles that already precipitated in the transported vesicles, what challenges the previous model of miliolid mineralization. Hence, Foraminifera probably utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls in both models are therefore most likely created by intravesicular accumulation of pre-formed liquid amorphous mineral phase deposited and crystallized within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well conserved in two clades that represent different chamber formation modes.

Effect of micro-plastic particles on coral reef foraminifera.

Foraminifera are single-celled protists which are important mediators of the marine carbon cycle. In our study, we explored the potential impact of polystyrene (PS) microplastic particles on two symbiont-bearing large benthic foraminifera species-Heterostegina depressa and Amphistegina lobifera-over a period of three weeks, employing three different approaches: investigating (1) stable isotope (SI) incorporation-via 13C- and 15N-labelled substrates-of the foraminifera to assess their metabolic activity, (2) photosynthetic efficiency of the symbiotic diatoms using imaging PAM fluorometry, and (3) microscopic enumeration of accumulation of PS microplastic particles inside the foraminiferal test. The active feeder A. lobifera incorporated significantly more PS particles inside the cytoplasm than the non-feeding H. depressa, the latter accumulating the beads on the test surface. Photosynthetic area of the symbionts tended to decrease in the presence of microplastic particles in both species, suggesting that the foraminiferal host cells started to digest their diatom symbionts. Compared to the control, the presence of microplastic particles lead to reduced SI uptake in A. lobifera, which indicates inhibition of inorganic carbon and nitrogen assimilation. Competition for particulate food uptake was demonstrated between algae and microplastic particles of similar size. Based on our results, both species seem to be sensitive to microplastic pollution, with non-feeding H. depressa being more strongly affected.

Unique evolution of foraminiferal calcification to survive global changes.

Foraminifera, the most ancient known calcium carbonate-producing eukaryotes, are crucial players in global biogeochemical cycles and well-used environmental indicators in biogeosciences. However, little is known about their calcification mechanisms. This impedes understanding the organismal responses to ocean acidification, which alters marine calcium carbonate production, potentially leading to biogeochemical cycle changes. We conducted comparative single-cell transcriptomics and fluorescent microscopy and identified calcium ion (Ca2+) transport/secretion genes and α-carbonic anhydrases that control calcification in a foraminifer. They actively take up Ca2+ to boost mitochondrial adenosine triphosphate synthesis during calcification but need to pump excess intracellular Ca2+ to the calcification site to prevent cell death. Unique α-carbonic anhydrase genes induce the generation of bicarbonate and proton from multiple CO2 sources. These control mechanisms have evolved independently since the Precambrian to enable the development of large cells and calcification despite decreasing Ca2+ concentrations and pH in seawater. The present findings provide previously unknown insights into the calcification mechanisms and their subsequent function in enduring ocean acidification.

The change in metabolic activity of a large benthic foraminifera as a function of light supply.

We studied metabolic activity of the symbiont-bearing large benthic foraminifer Heterostegina depressa under different light conditions. Besides the overall photosynthetic performance of the photosymbionts estimated by means of variable fluorescence, the isotope uptake (13C and 15N) of the specimens (= holobionts) was measured. Heterostegina depressa was either incubated in darkness over a period of 15 days or exposed to an 16:8 h light:dark cycle mimicking natural light conditions. We found photosynthetic performance to be highly related to light supply. The photosymbionts, however, survived prolonged darkness and could be reactivated after 15 days of darkness. The same pattern was found in the isotope uptake of the holobionts. Based on these results, we propose that 13C-carbonate and 15N-nitrate assimilation is mainly controlled by the photosymbionts, whereas 15N-ammonium and 13C-glucose utilization is regulated by both, the symbiont and the host cells.

Spectroscopic analysis of sequestered chloroplasts in Elphidium williamsoni (Foraminifera).

Foraminifera are unicellular, marine organisms that occur worldwide. A very common species in the German Wadden Sea is Elphidium williamsoni. Some foraminifera (such as elphidia) are able to use kleptoplastidy, which allows them to incorporate chloroplasts from their algal food source into their own cell body. The experiments reported here are based on the fact that chlorophyll (a and c) can be detected in the intact cells with spectroscopic methods in the visible spectral range, which allows an indirect investigation of the presence of sequestered chloroplasts. Starving experiments of E. williamsoni in the light (24 h continuous) showed that the greatest decrease in chlorophyll content was recorded within the first 20-30 days. From day 60 on, chlorophyll was hardly detectable. Through subsequent feeding on a renewed algal food source a significant increase in the chlorophyll content in foraminifera was noticed. The degradation of chlorophyll in the dark (24 h continuous darkness) during the starving period was much more complex. Chlorophyll was still detected in the cells after 113 days of starving time. Therefore, we hypotheses that the effect of photoinhibition applies to chloroplasts in foraminifera under continuous illumination.

Enhanced ocean oxygenation during Cenozoic warm periods.

Dissolved oxygen (O2) is essential for most ocean ecosystems, fuelling organisms' respiration and facilitating the cycling of carbon and nutrients. Oxygen measurements have been interpreted to indicate that the ocean's oxygen-deficient zones (ODZs) are expanding under global warming1,2. However, models provide an unclear picture of future ODZ change in both the near term and the long term3-6. The paleoclimate record can help explore the possible range of ODZ changes in warmer-than-modern periods. Here we use foraminifera-bound nitrogen (N) isotopes to show that water-column denitrification in the eastern tropical North Pacific was greatly reduced during the Middle Miocene Climatic Optimum (MMCO) and the Early Eocene Climatic Optimum (EECO). Because denitrification is restricted to oxygen-poor waters, our results indicate that, in these two Cenozoic periods of sustained warmth, ODZs were contracted, not expanded. ODZ contraction may have arisen from a decrease in upwelling-fuelled biological productivity in the tropical Pacific, which would have reduced oxygen demand in the subsurface. Alternatively, invigoration of deep-water ventilation by the Southern Ocean may have weakened the ocean's 'biological carbon pump', which would have increased deep-ocean oxygen. The mechanism at play would have determined whether the ODZ contractions occurred in step with the warming or took centuries or millennia to develop. Thus, although our results from the Cenozoic do not necessarily apply to the near-term future, they might imply that global warming may eventually cause ODZ contraction.

Denitrification in foraminifera has an ancient origin and is complemented by associated bacteria.

Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid Globobulimina spp. has been shown to encode an incomplete denitrification pathway of bacterial origin. However, the prevalence of denitrification genes in foraminifera remains unknown, and the missing denitrification pathway components are elusive. Analyzing transcriptomes and metagenomes of 10 foraminiferal species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer the last common ancestor of denitrifying foraminifera, which enables us to predict the ability to denitrify for additional foraminiferal species. Additionally, an examination of the foraminiferal microbiota reveals evidence for a stable interaction with Desulfobacteraceae, which harbor genes that complement the foraminiferal denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera-associated microbiome. The interaction of foraminifera with their resident bacteria is at the basis of foraminiferal adaptation to anaerobic environments that manifested in ecological success in oxygen depleted habitats.

Photosynthetic performance of symbiont-bearing foraminifera Heterostegina depressa affected by sunscreens.

Foraminifera are abundant unicellular organisms that play an important role in marine element cycles. A large benthic foraminifer obligatory bearing photosymbionts is Heterostegina depressa. We studied potential impacts of sunscreens available on the market on the activity of photosymbionts on H. depressa by means of pulse-amplitude modulated (PAM) fluorescence microscopy. We included four different sunscreens, with two of them sold as "conventional" and two more stated as "eco-friendly". Further, the impact of pure Ensulizole (phenylbenzimidazole sulfonic acid) was tested, which is a common agent of sunscreens. Foraminifera were incubated at varying concentrations (10, 50 and 200 mgL-1) of different sunscreens and the pure Ensulizole for 14 days. The photosynthetic performance was measured after 1,3, 7 and 14 days. Pure Ensulizole had a strong negative impact on the photobionts, which was reflected by a significant reduction of the areal fluorescence signal. "Eco-friendly" sunscreens affected the health of foraminifera more severely compared to "conventional" ones. We assume that metal nanoparticles like titanium dioxide or zinc oxide of "eco-friendly" sunscreens are causing this impact, because these substances were already classified as toxic for several microorganisms.

Influence of methane seepage on isotopic signatures in living deep-sea benthic foraminifera, 79° N.

Fossil benthic foraminifera are used to trace past methane release linked to climate change. However, it is still debated whether isotopic signatures of living foraminifera from methane-charged sediments reflect incorporation of methane-derived carbon. A deeper understanding of isotopic signatures of living benthic foraminifera from methane-rich environments will help to improve reconstructions of methane release in the past and better predict the impact of future climate warming on methane seepage. Here, we present isotopic signatures (δ13C and δ18O) of foraminiferal calcite together with biogeochemical data from Arctic seep environments from c. 1200 m water depth, Vestnesa Ridge, 79° N, Fram Strait. Lowest δ13C values were recorded in shells of Melonis barleeanus, - 5.2‰ in live specimens and - 6.5‰ in empty shells, from sediments dominated by aerobic (MOx) and anaerobic oxidation of methane (AOM), respectively. Our data indicate that foraminifera actively incorporate methane-derived carbon when living in sediments with moderate seepage activity, while in sediments with high seepage activity the poisonous sulfidic environment leads to death of the foraminifera and an overgrowth of their empty shells by methane-derived authigenic carbonates. We propose that the incorporation of methane-derived carbon in living foraminifera occurs via feeding on methanotrophic bacteria and/or incorporation of ambient dissolved inorganic carbon.

Shell density of planktonic foraminifera and pteropod species Limacina helicina in the Barents Sea: Relation to ontogeny and water chemistry.

Planktonic calcifiers, the foraminiferal species Neogloboquadrina pachyderma and Turborotalita quinqueloba, and the thecosome pteropod Limacina helicina from plankton tows and surface sediments from the northern Barents Sea were studied to assess how shell density varies with depth habitat and ontogenetic processes. The shells were measured using X-ray microcomputed tomography (XMCT) scanning and compared to the physical and chemical properties of the water column including the carbonate chemistry and calcium carbonate saturation of calcite and aragonite. Both living L. helicina and N. pachyderma increased in shell density from the surface to 300 m water depth. Turborotalita quinqueloba increased in shell density to 150-200 m water depth. Deeper than 150 m, T. quinqueloba experienced a loss of density due to internal dissolution, possibly related to gametogenesis. The shell density of recently settled (dead) specimens of planktonic foraminifera from surface sediment samples was compared to the living fauna and showed a large range of dissolution states. This dissolution was not apparent from shell-surface texture, especially for N. pachyderma, which tended to be both thicker and denser than T. quinqueloba. Dissolution lowered the shell density while the thickness of the shell remained intact. Limacina helicina also increase in shell size with water depth and thicken the shell apex with growth. This study demonstrates that the living fauna in this specific area from the Barents Sea did not suffer from dissolution effects. Dissolution occurred after death and after settling on the sea floor. The study also shows that biomonitoring is important for the understanding of the natural variability in shell density of calcifying zooplankton.

Effects of temperature on the behaviour and metabolism of an intertidal foraminifera and consequences for benthic ecosystem functioning.

Heatwaves have increased in intensity, duration and frequency over the last decades due to climate change. Intertidal species, living in a highly variable environment, are likely to be exposed to such heatwaves since they can be emerged for more than 6 h during a tidal cycle. Little is known, however, on how temperature affects species traits (e.g. locomotion and behaviour) of slow-moving organisms such as benthic foraminifera (single-celled protists), which abound in marine sediments. Here, we examine how temperature influences motion-behaviour and metabolic traits of the dominant temperate foraminifera Haynesina germanica by exposing individuals to usual (6, 12, 18, 24, 30 °C) and extreme (high; i.e. 32, 34, 36 °C) temperature regimes. Our results show that individuals reduced their activity by up to 80% under high temperature regimes whereas they remained active under the temperatures they usually experience in the field. When exposed to a hyper-thermic stress (i.e. 36 °C), all individuals remained burrowed and the photosynthetic activity of their sequestered chloroplasts significantly decreased. Recovery experiments subsequently revealed that individuals initially exposed to a high thermal regime partially recovered when the hyper-thermic stress ceased. H. germanica contribution to surface sediment reworking substantially diminished from 10 mm3 indiv-1 day-1 (usual temperature) to 0 mm3 indiv-1 day-1 when individuals were exposed to high temperature regimes (i.e. above 32 °C). Given their role in sediment reworking and organic matter remineralisation, our results suggest that heatwaves may have profound long-lasting effects on the functioning of intertidal muddy ecosystems and some key biogeochemical cycles.

Relationship between individual chamber and whole shell Mg/Ca ratios in Trilobatus sacculifer and implications for individual foraminifera palaeoceanographic reconstructions.

Precisely targeted measurements of trace elements using laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS) reveal inter-chamber heterogeneities in specimens of the planktic foraminifer Trilobatus (Globigerinoides) sacculifer. We find that Mg/Ca ratios in the final growth chamber are generally lower compared to previous growth chambers, but final chamber Mg/Ca is elevated in one of thirteen sample intervals. Differences in distributions of Mg/Ca values from separate growth chambers are observed, occurring most often at lower Mg/Ca values, suggesting that single-chamber measurements may not be reflective of the specimen's integrated Mg/Ca. We compared LA-ICPMS Mg/Ca values to paired, same-individual Mg/Ca measured via inductively coupled plasma optical emission spectrometry (ICP-OES) to assess their correspondence. Paired LA-ICPMS and ICP-OES Mg/Ca show a maximum correlation coefficient of R = 0.92 (p < 0.05) achieved by applying a weighted average of the last and penultimate growth chambers. Population distributions of paired Mg/Ca values are identical under this weighting. These findings demonstrate that multi-chamber LA-ICPMS measurements can approximate entire specimen Mg/Ca, and is thus representative of the integrated conditions experienced during the specimen's lifespan. This correspondence between LA-ICPMS and ICP-OES data links these methods and demonstrates that both generate Mg/Ca values suitable for individual foraminifera palaeoceanographic reconstructions.

Nanoscale trace metal imprinting of biocalcification of planktic foraminifers by Toba's super-eruption.

Bioactive metal releases in ocean surface water, such as those by ash falls during volcanic super-eruptions, might have a potentially toxic impact on biocalcifier planktic microorganisms. Nano-XRF imaging with the cutting-edge synchrotron hard X-ray nano-analysis ID16B beamline (ESRF) revealed for the first time a specific Zn- and Mn-rich banding pattern in the test walls of Globorotalia menardii planktic foraminifers extracted from the Young Toba Tuff layer, and thus contemporaneous with Toba's super-eruption, 74,000 years ago. The intra-test correlation of Zn and Mn patterns at the nanoscale with the layered calcareous microarchitecture, indicates that the incorporation of these metals is syngenetic to the wall growth. The preferential Mn and Zn sequestration within the incipient stages of chamber formation suggests a selective incorporation mechanism providing a resilience strategy to metal pollution in the test building of planktic foraminifers.

The effect of long-term brine discharge from desalination plants on benthic foraminifera.

Desalination plants along the Mediterranean Israeli coastline currently provide ~587 million m3 drinking water/year, and their production is planned to increase gradually. Production of drinking water is accompanied by a nearly equivalent volume of brine discharge with a salinity of ~80 that is twice the normal, which can potentially impact marine ecosystems. The goal of this study was to examine whether benthic foraminifera, a known sensitive marine bio-indicator, are affected by this brine-discharge. For that, we investigated the seasonal and cumulative effect of brine discharges of three operating desalination facilities along the Israeli coast. Those facilities are located in Ashkelon, Hadera, and Sorek. The brine-discharge in the first two desalination plants is associated with thermal pollution, while the Sorek facility entails increased salinity but no thermal pollution. In four seasonal cruises during one year, we collected surface sediment samples in triplicates by grabs from the outfall (near the discharge site), and from a non-impacted control station adjacent to each study site. Our results highlight that the most robust responses were observed at two out of three desalination shallow sites (Ashkelon and Hadera), where the brine was discharged directly from a coastal outfall and was accompanied with thermal pollution from the nearby power plants. The total foraminiferal abundance and diversity were, generally, lower near the outfalls, and increased towards the control stations. Moreover, changes in the relative abundances of selected species indicate their sensitivity to the brine discharge. The most noticeable response to exclusively elevated salinity was detected at Sorek discharge site, where we observed a sharp decline in organic-cemented agglutinated benthic foraminifera, suggesting that these are particularly sensitive to elevated salinity. The herein study contribute new insights into the effect of brine discharge from desalination plants, on benthic foraminifera, and propose a scientifically-based ecological monitoring tool that can help stakeholders.

Rapid ocean acidification and protracted Earth system recovery followed the end-Cretaceous Chicxulub impact.

Mass extinction at the Cretaceous-Paleogene (K-Pg) boundary coincides with the Chicxulub bolide impact and also falls within the broader time frame of Deccan trap emplacement. Critically, though, empirical evidence as to how either of these factors could have driven observed extinction patterns and carbon cycle perturbations is still lacking. Here, using boron isotopes in foraminifera, we document a geologically rapid surface-ocean pH drop following the Chicxulub impact, supporting impact-induced ocean acidification as a mechanism for ecological collapse in the marine realm. Subsequently, surface water pH rebounded sharply with the extinction of marine calcifiers and the associated imbalance in the global carbon cycle. Our reconstructed water-column pH gradients, combined with Earth system modeling, indicate that a partial ∼50% reduction in global marine primary productivity is sufficient to explain observed marine carbon isotope patterns at the K-Pg, due to the underlying action of the solubility pump. While primary productivity recovered within a few tens of thousands of years, inefficiency in carbon export to the deep sea lasted much longer. This phased recovery scenario reconciles competing hypotheses previously put forward to explain the K-Pg carbon isotope records, and explains both spatially variable patterns of change in marine productivity across the event and a lack of extinction at the deep sea floor. In sum, we provide insights into the drivers of the last mass extinction, the recovery of marine carbon cycling in a postextinction world, and the way in which marine life imprints its isotopic signal onto the geological record.

Lunar cycles and rainy seasons drive growth and reproduction in nummulitid foraminifera, important producers of carbonate buildups.

Representatives of the foraminifer Nummulites are important in Earth history for timing Cenozoic shallow-water carbonates. Taphonomic complexity explains the construction of carbonate buildups, but reproduction and life span of the constructing individuals are unknown. During the 15-month investigation period, asexually reproduced schizonts and gamonts showed equal proportions in the first half of this period, whereas gamonts predominated in the second half. Oscillations in cell growth are mainly caused by light intensities during chamber construction when minor differences in water depth increase the photosynthetic rate of endosymbiotic diatoms during neap tides. The continuous reproduction rate of N. venosus throughout the year is increased in subtropical calms by higher summer temperatures and the marginal input of inorganic nutrients during rainy seasons. The expected life span of both gamonts and schizonts are 18 months.

Scaling laws explain foraminiferal pore patterns.

Due to climate warming and increased anthropogenic impact, a decrease of ocean water oxygenation is expected in the near future, with major consequences for marine life. In this context, it is essential to develop reliable tools to assess past oxygen concentrations in the ocean, to better forecast these future changes. Recently, foraminiferal pore patterns have been proposed as a bottom water oxygenation proxy, but the parameters controlling foraminiferal pore patterns are still largely unknown. Here we use scaling laws to describe how both gas exchanges (metabolic needs) and mechanical constraints (shell robustness) control foraminiferal pore patterns. The derived mathematical model shows that only specific combinations of pore density and size are physically feasible. Maximum porosity, of about 30%, can only be obtained by simultaneously increasing pore size and decreasing pore density. A large empirical data set of pore data obtained for three pseudocryptic phylotypes of Ammonia, a common intertidal genus from the eastern Atlantic, strongly supports this conclusion. These new findings provide basic mechanistic understanding of the complex controls of foraminiferal pore patterns and give a solid starting point for the development of proxies of past oxygen concentrations based on these morphological features. Pore size and pore density are largely interdependent, and both have to be considered when describing pore patterns.

Response of a kleptoplastidic foraminifer to heterotrophic starvation: photosynthesis and lipid droplet biogenesis.

The aim of this work is to document the complex nutritional strategy developed by kleptoplastic intertidal foraminifera. We study the mixotrophic ability of a common intertidal foraminifer, Elphidium williamsoni, by (i) investigating the phylogenetic identity of the foraminiferal kleptoplasts, (ii) following their oxygenic photosynthetic capacity and (iii) observing the modification in cellular ultrastructural features in response to photoautotrophic conditions. This was achieved by coupling molecular phylogenetic analyses and TEM observations with non-destructive measurements of kleptoplast O2 production over a 15-day experimental study. Results show that the studied E. williamsoni actively selected kleptoplasts mainly from pennate diatoms and had the ability to produce oxygen, up to 13.4 nmol O2 cell-1 d-1, from low to relatively high irradiance over at least 15 days. Ultrastructural features and photophysiological data showed significant differences over time, the number of lipid droplets, residual bodies and the dark respiration increased; whereas, the number of kleptoplasts decreased accompanied by a minor decrease of the photosynthetic rate. These observations suggest that in E. williamsoni kleptoplasts might provide extra carbon storage through lipid droplets synthesis and highlight the complexity of E. williamsoni feeding strategy and the necessity of further dedicated studies regarding mechanisms developed by kleptoplastidic foraminifera for carbon partitioning and storage.

Advanced approach to analyzing calcareous protists for present and past pelagic ecology: Comprehensive analysis of 3D-morphology, stable isotopes, and genes of planktic foraminifers.

Marine protists play an important role in oceanic ecosystems and biogeochemical cycles. However, the difficulties in culturing pelagic protists indicate that their ecology and behavior remain poorly understood; phylogeographic studies based on single-cell genetic analyses have often shown that they are highly divergent at the biological species level, with variable geographic distributions. This indicates that their ecology could be complex. On the other hand, the biomineral (calcareous) shells of planktic foraminifers are widely used in geochemical analyses to estimate marine paleoenvironmental characteristics (i.e., temperature), because the shell chemical composition reflects ambient seawater conditions. Among the pelagic protists, planktic foraminifers are ideal study candidates to develop a combined approach of genetic, morphological, and geochemical methods, thus reflecting environmental and ecological characteristics. The present study precisely tested whether the DNA extraction process physically and chemically affects the shells of the planktic foraminifer Globigerinoides ruber. We used a nondestructive method for analyzing physical changes (micro-focus X-ray computed tomography (MXCT) scanning) to compare specimens at the pre- and post-DNA extraction stages. Our results demonstrate that DNA extraction has no significant effect on shell density and thickness. We measured stable carbon and oxygen isotopes on the shell of each individual in a negative control or one of two DNA-extracted groups and detected no significant differences in isotopic values among the three groups. Moreover, we evaluated isotopic variations at the biological species level with regard to their ecological characteristics such as depth habitat, life stages, and symbionts. Thus, our examination of the physiochemical effects on biomineral shells through DNA extraction shows that morphological and isotopic analyses of foraminifers can be combined with genetic analysis. These analytical methods are applicable to other shell-forming protists and microorganisms. In this study, we developed a powerful analytical tool for use in ecological and environmental studies of modern and past oceans.

Form and function of F-actin during biomineralization revealed from live experiments on foraminifera.

Although the emergence of complex biomineralized forms has been investigated for over a century, still little is known on how single cells control morphology of skeletal structures, such as frustules, shells, spicules, or scales. We have run experiments on the shell formation in foraminifera, unicellular, mainly marine organisms that can build shells by successive additions of chambers. We used live imaging to discover that all stages of chamber/shell formation are controlled by dedicated actin-driven pseudopodial structures. Successive reorganization of an F-actin meshwork, associated with microtubular structures, is actively involved in formation of protective envelope, followed by dynamic scaffolding of chamber morphology. Then lamellar dynamic templates create a confined space and control mineralization separated from seawater. These observations exclude extracellular calcification assumed in selected foraminiferal clades, and instead suggest a semiintracellular biomineralization pattern known from other unicellular calcifying and silicifying organisms. These results give a challenging prospect to decipher the vital effect on geochemical proxies applied to paleoceanographic reconstructions. They have further implications for understanding multiscale complexity of biomineralization and show a prospect for material science applications.