Project description:We report nuclear small-subunit rDNA sequences for two species of the benthic foraminifer Ammonia. Because of their abundance in present and past seas, the foraminifera are a very important group of organisms used in a wide range of geologic studies; however, the ancestry of this group was, until now, unknown. Difficulties in purifying foraminiferal DNA and avoiding PCR contamination led us to develop DNA.DNA in situ hybridization techniques to verify our sequence data. Phylogenetic analysis of verified foraminiferal DNA sequence indicates these taxa are a divergent, "alveolate" lineage, within the major eukaryotic radiation. Our findings cast doubt upon the assumption that all foraminifera are derived from an amoebalike ancestor. Cytological features and the DNA sequences presented herein suggest that the foraminifera were derived from a heterokaryotic flagellated marine protist, probably sometime in the later Proterozoic.
Project description:The association with photosymbiotic algae is crucial for the proliferation of many coral reef organisms, but increases their sensitivity to environmental changes. Large benthic foraminifera (LBF) are a diverse group of carbonate producers harboring algal photosymbionts. They act as key ecological engineers and are widely used as bioindicators. As in corals, elevated temperatures and light intensities are known to induce bleaching in LBF, but the combined effects of ocean acidification and warming remain unclear. To shed light into the adaptive physiology of LBF, we linked the assessment of the holobiont and photosymbiont physiological condition (mortality, growth, coloration, and chlorophyll a) to a bottom-up proteomics approach that allows the examination of cellular responses of host and symbionts simultaneously. In a two-months experiment, we exposed Amphistegina lobifera to the combined effects of ocean acidification (400, 1000 and 2800 ppm pCO2) and warming (28-control and 31°C). More than 1,000 proteins were identified by label-free mass spectrometry-based whole proteome analysis and assigned to the host or photosymbionts. Photopigment concentrations declined in response to elevated pCO2, visible by discoloration. These indicate the reduction of photosymbiont densities under ocean acidification, despite the fertilizing effects suggested for high inorganic carbon availability, and imply metabolic adjustments. Increases of proteolytic proteins suggest active host regulation of photosymbiont density in order to maintain homeostasis with its algal photosymbionts. Growth rates, however, were unaffected by elevated pCO2 levels at control temperatures, but high pCO2 levels (2800 ppm, pH 7.52) combined with thermal stress (31°C) impaired growth, though mortality and shell dissolution was negligible. While growth was unaffected by intermediate pCO2 levels (1000 ppm, pH 7.98) combined with ocean warming, this treatment induced the most distinct proteome responses. These include the regulation of ion transporters and host cytoplasmic proteins that likely abet calcification under ocean acidification. This study reveals a highly complex cellular response in both the host and the photosymbiont, which appears to facilitate a high resilience potential of A. lobifera to end of the century ocean conditions. Nevertheless, our results imply that when pCO2 levels rise above 1000 ppm during persistent ocean warming or extreme heating events these adaptive mechanisms become disrupted.
Project description:Fossil Foraminifera appear in the Early Cambrian, at about the same time as the first skeletonized metazoans. However, due to the inadequate preservation of early unilocular (single-chambered) foraminiferal tests and difficulties in their identification, the evolution of early foraminifers is poorly understood. By using molecular data from a wide range of extant naked and testate unilocular species, we demonstrate that a large radiation of nonfossilized unilocular Foraminifera preceded the diversification of multilocular lineages during the Carboniferous. Within this radiation, similar test morphologies and wall types developed several times independently. Our findings indicate that the early Foraminifera were an important component of Neoproterozoic protistan community, whose ecological complexity was probably much higher than has been generally accepted.
Project description: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.
Project description:This work shows that calcareous benthic foraminifera are capable of agglutinating sedimentary particles also. In particular, we focus on Melonis barleeanus. Traditionally considered a calcareous species, our data revealed the presence of minute (~3 μm) sedimentary particles (silicate grains) inside the chamber walls of the examined shells. These particles were arranged in a definitive and systematic pattern, and the similar grain chemical characterization and size suggested a relatively high degree of selectivity in both modern and fossil specimens. Based on these results, we propose that M. barleeanus is capable of agglutinating sedimentary particles during the formation of a new chamber. The analysis of other calcareous foraminiferal species (e.g., Cassidulina neoteretis, Lobatula lobatula, Nonionella stella) did not reveal the presence of silicate grains in the shell of the specimens analyzed confirming this to be a characteristic of M. barleeanus. Considering that the isotopic and chemical composition of this species is widely used in paleoclimatic and paleoceanographic reconstructions, we used a mixing model to better constrain the influence of sedimentary particles on M. barleeanus δ18O data. Our model showed that the calcite δ18O would increase by ~0.9-2‰ if 10 wt% of feldspars (i.e., anorthite, albite, orthoclase) and quartz, respectively, were included in the analyzed shell. Based on these results, we emphasize that it is of paramount importance to consider M. barleeanus unusual biomineralization strategy during the interpretation of geological records and to investigate the presence of similar processes in other calcareous foraminiferal species.
Project description:Benthic foraminifera are unicellular eukaryotes inhabiting sediments of aquatic environments. Several species were shown to store and use nitrate for complete denitrification, a unique energy metabolism among eukaryotes. The population of benthic foraminifera reaches high densities in oxygen-depleted marine habitats, where they play a key role in the marine nitrogen cycle. However, the mechanisms of denitrification in foraminifera are still unknown, and the possibility of a contribution of associated bacteria is debated. Here, we present evidence for a novel eukaryotic denitrification pathway that is encoded in foraminiferal genomes. Large-scale genome and transcriptomes analyses reveal the presence of a denitrification pathway in foraminifera species of the genus Globobulimina. This includes the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrate transporters (Nrt). A phylogenetic reconstruction of the enzymes' evolutionary history uncovers evidence for an ancient acquisition of the foraminiferal denitrification pathway from prokaryotes. We propose a model for denitrification in foraminifera, where a common electron transport chain is used for anaerobic and aerobic respiration. The evolution of hybrid respiration in foraminifera likely contributed to their ecological success, which is well documented in palaeontological records since the Cambrian period.
Project description:Nitrogen availability often limits biological productivity in marine systems, where inorganic nitrogen, such as ammonium is assimilated into the food web by bacteria and photoautotrophic eukaryotes. Recently, ammonium assimilation was observed in kleptoplast-containing protists of the phylum foraminifera, possibly via the glutamine synthetase/glutamate synthase (GS/GOGAT) assimilation pathway imported with the kleptoplasts. However, it is not known if the ubiquitous and diverse heterotrophic protists have an innate ability for ammonium assimilation. Using stable isotope incubations (15N-ammonium and 13C-bicarbonate) and combining transmission electron microscopy (TEM) with quantitative nanoscale secondary ion mass spectrometry (NanoSIMS) imaging, we investigated the uptake and assimilation of dissolved inorganic ammonium by two heterotrophic foraminifera; a non-kleptoplastic benthic species, Ammonia sp., and a planktonic species, Globigerina bulloides. These species are heterotrophic and not capable of photosynthesis. Accordingly, they did not assimilate 13C-bicarbonate. However, both species assimilated dissolved 15N-ammonium and incorporated it into organelles of direct importance for ontogenetic growth and development of the cell. These observations demonstrate that at least some heterotrophic protists have an innate cellular mechanism for inorganic ammonium assimilation, highlighting a newly discovered pathway for dissolved inorganic nitrogen (DIN) assimilation within the marine microbial loop.
Project description:Sargassum is one of the most diverse brown algal genus with more than 150 known species, mostly benthic and few pelagic species. They contribute significantly to global primary production and serve as important habitat for wide range of marine organisms. Sargassum vulgare is one of the dominant habitat forming species along Mediterranean coast. Despite their huge ecological importance, it is relatively unknown how they will respond under future global climate change scenario. This work used de novo transcriptome sequencing approach to understand the molecular response of S. vulgare to chronic acidification at the shallow underwater volcanic CO2 vents off Ischia Island, Italy. Keywords: brown algae, Sargassum, de novo transcriptome, ocean acidification, CO2 vents.