Lennart Jan de Nooijer

Foraminifera promote calcification by elevating their intracellular pH

Surface seawaters are supersaturated with respect to calcite, but high concentrations of magnesium prevent spontaneous nucleation and growth of crystals. Foraminifera are the most widespread group of calcifying organisms and generally produce calcite with a low Mg content, indicating that they actively remove Mg2+ from vacuolized seawater before calcite precipitation. However, one order of foraminifera has evolved a calcification pathway, by which it produces calcite with a very high Mg content, suggesting that these species do not alter the Mg/Ca ratio of vacuolized seawater considerably. The cellular mechanism that makes it possible to precipitate calcite at high Mg concentrations, however, has remained unknown. Here we demonstrate that they are able to elevate the pH at the site of calcification by at least one unit above seawater pH and, thereby, overcome precipitation-inhibition at ambient Mg concentrations. A similar result was obtained for species that precipitate calcite with a low Mg concentration, suggesting that elevating the pH at the site of calcification is a widespread strategy among foraminifera to promote calcite precipitation. Since the common ancestor of these two groups dates back to the Cambrian, our results would imply that this physiological mechanism has evolved over half a billion years ago. Since foraminifera rely on elevating the intracellular pH for their calcification, our results show that ongoing ocean acidification can result in a decrease of calcite production by these abundant calcifyers.

Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania Huxleyi (haptophyta) and reflect specialization to different ecological niches

Coccolithophores, especially the abundant, cosmopolitan species Emiliania huxleyi (Lohmann) W. W. Hay et H. P. Mohler, are one of the main driving forces of the oceanic carbonate pump and contribute significantly to global carbon cycling, due to their ability to calcify. A recent study indicates that termination of diploid blooms by viral infection induces life‐cycle transition, and speculation has arisen about the role of the haploid, noncalcifying stage in coccolithophore ecology. To explore gene expression patterns in both life‐cycle stages, haploid and diploid cells of E. huxleyi (RCC 1217 and RCC 1216) were acclimated to limiting and saturating photon flux densities. Transcriptome analyses were performed to assess differential genomic expression related to different ploidy levels and acclimation light intensities. Analyses indicated that life‐cycle stages exhibit different properties of regulating genome expression (e.g., pronounced gene activation and gene silencing in the diploid stage), proteome maintenance (e.g., increased turnover of proteins in the haploid stage), as well as metabolic processing (e.g., pronounced primary metabolism and motility in the haploid stage and calcification in the diploid stage). Furthermore, higher abundances of transcripts related to endocytotic and digestive machinery were observed in the diploid stage. A qualitative feeding experiment indicated that both life‐cycle stages are capable of particle uptake (0.5 μm diameter) in late‐stationary growth phase. Results showed that the two life‐cycle stages represent functionally distinct entities that are evolutionarily shaped to thrive in the environment they typically inhabit.

Incorporation of uranium in benthic foraminiferal calcite reflects seawater carbonate ion concentration

The chemical and isotopic composition of foraminiferal shells (so-called proxies) reflects the physico-chemical properties of the seawater. In current day paleoclimate research, the reconstruction of past seawater carbonate system to infer atmospheric CO2 concentrations is one of the most pressing challenges and a variety of proxies have been investigated, such as foraminiferal U/Ca. Since in natural seawater and traditional CO2 perturbation experiments, the carbonate system parameters co-vary, it is not possible to determine the parameter of the carbonate system causing e.g. changes in U/Ca, complicating the use of the latter as a carbonate system proxy. We overcome this problem, by culturing the benthic foraminifer Ammonia sp. at a range of carbonate chemistry manipulation treatments. Shell U/Ca values were determined to test sensitivity of U incorporation to various parameters of the carbonate system. We argue that [CO32-] is the parameter affecting the U/Ca ratio and consequently, the partitioning coefficient for U in Ammonia sp DU. We can confirm the strong potential of foraminiferal U/Ca as a [CO32-] proxy.

On the role of the cytoskeleton in coccolith morphogenesis: the effect of cytoskeleton inhibitors

The coccolithophore Emiliania huxleyi (Lohmann) W. W. Hay et H. Mohler was cultured in natural seawater with the addition of either the microtubule‐inhibitor colchicine, the actin‐inhibitor cytochalasin B, or the photosynthesis inhibitor 3‐(3,4 dichlorophenyl)‐1,1‐dimethyl‐urea (DCMU). Additionally, E. huxleyi was cultured at different light intensities and temperatures. Growth rate was monitored, and coccolith morphology analyzed. While every treatment affected growth rate, the percentage of malformed coccoliths increased with colchicine, cytochalasin B, and at higher than optimal temperature. These results represent the first experimental evidence for the role of microtubules and actin microfilaments in coccolith morphogenesis.

Proton pumping accompanies calcification in foraminifera

Ongoing ocean acidification is widely reported to reduce the ability of calcifying marine organisms to produce their shells and skeletons. Whereas increased dissolution due to acidification is a largely inorganic process, strong organismal control over biomineralization influences calcification and hence complicates predicting the response of marine calcifyers. Here we show that calcification is driven by rapid transformation of bicarbonate into carbonate inside the cytoplasm, achieved by active outward proton pumping. Moreover, this proton flux is maintained over a wide range of pCO2 levels. We furthermore show that a V-type H+ ATPase is responsible for the proton flux and thereby calcification. External transformation of bicarbonate into CO2 due to the proton pumping implies that biomineralization does not rely on availability of carbonate ions, but total dissolved CO2 may not reduce calcification, thereby potentially maintaining the current global marine carbonate production.

Profiling planktonic foraminiferal crust formation

Planktonic foraminifera migrate vertically through the water column during their life, thereby growing and calcifying over a range of depth-associated conditions. Some species form a calcite veneer, crust, or cortex at the end of their lifecycle. This additional calcite layer may vary in structure, composition, and thickness, potentially accounting for most of their total shell mass and thereby dominating the element and isotope signature of the whole shell. Here we apply laser ablation ICP-MS depth profiling to assess variability in thickness and Mg/Ca composition of shell walls of three encrusting species derived from sediment traps. Compositionally, Mg/Ca is significantly lower in the crusts of Neogloboquadrina dutertrei and Globorotalia scitula, as well as in the cortex of Pulleniatina obliquiloculata, independent of the species-specific Mg/Ca of their lamellar calcite shell. Wall thickness accounts for nearly half of the total thickness in both crustal species and nearly a third in cortical P. obliquiloculata, regardless of their initial shell wall thickness. Crust thickness and crustal Mg/Ca decreases toward the younger chambers in N. dutertrei and to a lesser extent, also in G. scitula. In contrast, the cortex of P. obliquiloculata shows a nearly constant thickness and uniform Mg/Ca through the complete chamber wall. Patterns in thickness and Mg/Ca of the crust indicate that temperature is not the dominant factor controlling crust formation. Instead, we present a depth-resolved model explaining compositional differences within individuals and between successive chambers as well as compositional heterogeneity of the crust and lamellar calcite in all three species studied here.

Unexpected biotic resilience on the Japanese seafloor caused by the 2011 Tohoku-Oki tsunami

On March 11th, 2011 the Mw 9.0 2011 Tōhoku-Oki earthquake resulted in a tsunami which caused major devastation in coastal areas. Along the Japanese NE coast, tsunami waves reached maximum run-ups of 40 m, and travelled kilometers inland. Whereas devastation was clearly visible on land, underwater impact is much more difficult to assess. Here, we report unexpected results obtained during a research cruise targeting the seafloor off Shimokita (NE Japan), shortly (five months) after the disaster. The geography of the studied area is characterized by smooth coastline and a gradually descending shelf slope. Although high-energy tsunami waves caused major sediment reworking in shallow-water environments, investigated shelf ecosystems were characterized by surprisingly high benthic diversity and showed no evidence of mass mortality. Conversely, just beyond the shelf break, the benthic ecosystem was dominated by a low-diversity, opportunistic fauna indicating ongoing colonization of massive sand-bed deposits.