Experimental determination of carbonate-associated sulfate δ^(34)S in planktonic foraminifera shells

Understanding the coupling of oxygen, carbon, and sulfur cycles in the past is critical for reconstructing the history of biogeochemical cycles, paleoclimatic variations, and oceanic chemistry. The abundance of sulfur isotopes (δ^(34)S) in sulfate from ancient marine carbonates, or carbonate-associated sulfate (CAS), is commonly used, along with other archives (mainly evaporites and barite), to estimate the δ^(34)S of seawater throughout Earth history. Analyses of CAS from hand-picked foraminifera are potentially valuable because this group of organisms is used in numerous paleoceanographic studies. They could provide coupled, high-resolution records of δ^(13)C, δ^(18)O, and δ^(34)S isotopic changes directly linked to orbitally tuned records of climate change through the Cenozoic. Such measurements have not previously been possible due to limitations of sensitivity in conventional IRMS-based techniques. However, the recent development of CAS analysis by multicollector inductively coupled plasma mass spectrometry (MC-ICP-MS) now allows us to work on samples containing just a few nmol of sulfur with accuracy for δ^(34)S values approaching 0.1‰ and, consequently, to analyze hand-picked samples of foraminifera shells. Here we report the results of culture experiments with the planktonic species Orbulina universa, that establish a shell:seawater δ^(34)S calibration for future applications to the fossil record. Our new method uses <650 μg of carbonate (∼15 shells) per analysis. The results show that S isotopes are fractionated consistently by −1‰ between seawater and O. universa tests. We also demonstrate that O. universa faithfully records the [SO^(2−)_(4)]/[Ca^(2+)] ratio of the seawater in which it grew

Nanometer-Scale Chemistry of a Calcite Biomineralization Template: Implications for Skeletal Composition and Nucleation

Plankton, corals, and other organisms produce calcium carbonate skeletons that are integral to their survival, form a key component of the global carbon cycle, and record an archive of past oceanographic conditions in their geochemistry. A key aspect of the formation of these biominerals is the interaction between organic templating structures and mineral precipitation processes. Laboratory-based studies have shown that these atomic-scale processes can profoundly influence the architecture and composition of minerals, but their importance in calcifying organisms is poorly understood because it is difficult to measure the chemistry of in vivo biomineral interfaces at spatially relevant scales. Understanding the role of templates in biomineral nucleation, and their importance in skeletal geochemistry requires an integrated, multiscale approach, which can place atom-scale observations of organic-mineral interfaces within a broader structural and geochemical context. Here we map the chemistry of an embedded organic template structure within a carbonate skeleton of the foraminifera Orbulina universa using both atom probe tomography (APT), a 3D chemical imaging technique with Angström-level spatial resolution, and time-of-flight secondary ionization mass spectrometry (ToF-SIMS), a 2D chemical imaging technique with submicron resolution. We quantitatively link these observations, revealing that the organic template in O. universa is uniquely enriched in both Na andMg, and contributes to intraskeletal chemical heterogeneity. Our APT analyses reveal the cation composition of the organic surface, offering evidence to suggest that cations other than Ca2+, previously considered passive spectator ions in biomineral templating, may be important in defining the energetics of carbonate nucleation on organic template

Planktonic foraminiferal assemblages reflect warming during two recent mid-latitude marine heatwaves

Under future climate scenarios, ocean temperatures that are presently extreme and qualify as marine heatwaves (MHW) are forecasted to increase in frequency and intensity, but little is known about the impact of these events on one of the most common paleoproxies, planktonic foraminifera. Planktonic foraminifera are globally ubiquitous, shelled marine protists. Their abundances and geochemistry vary with ocean conditions and fossil specimens are commonly used to reconstruct ancient ocean conditions. Planktonic foraminiferal assemblages are known to vary globally with sea surface temperature, primary productivity, and other hydrographic conditions, but have not been studied in the context of mid-latitude MHWs. For this study, the community composition and abundance of planktonic foraminifera were quantified for 2010-2019 along the Newport Hydrographic Line, a long-term monitoring transect at 44.6°N in the Northern California Current (NCC). Samples were obtained from archived plankton tows spanning 46 to 370 km offshore during annual autumn (August – October) cruises. Two MHWs impacted the region during this timeframe: the first during 2014-2016 and a second, shorter duration MHW in 2019. During the 2014-2016 MHW, warm water subtropical and tropical foraminifera species were more prevalent than the typical polar, subpolar, and transitional species common to this region. Cold water species were abundant again after the first MHW dissipated in late 2016. During the second, shorter-duration MHW in 2019, the assemblage consisted of a warm water assemblage but did not include tropical species. The foraminiferal assemblage variability correlated with changes in temperature and salinity in the upper 100 meters and was not correlated with distance offshore or upwelling. These results suggest that fossil foraminiferal assemblages from deep sea sediment cores may provide insight into the magnitude and frequency of past MHWs

Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

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

16S rRNA gene metabarcoding and TEM reveals different ecological strategies within the genus Neogloboquadrina (planktonic foraminifer)

CB was supported on a Daphne Jackson Fellowship sponsored by Natural Environmental Research Council (www.nerc.ac.uk) and the University of Edinburgh via the Daphne Jackson Trust. Field collections were supported by the National Science Foundation (www.nsf.gov) grant number OCE-1261519 to ADR and JSF.Uncovering the complexities of trophic and metabolic interactions among microorganisms is essential for the understanding of marine biogeochemical cycling and modelling climate-driven ecosystem shifts. High-throughput DNA sequencing methods provide valuable tools for examining these complex interactions, although this remains challenging, as many microorganisms are difficult to isolate, identify and culture. We use two species of planktonic foraminifera from the climatically susceptible, palaeoceanographically important genus Neogloboquadrina, as ideal test microorganisms for the application of 16S rRNA gene metabarcoding. Neogloboquadrina dutertrei and Neogloboquadrina incompta were collected from the California Current and subjected to either 16S rRNA gene metabarcoding, fluorescence microscopy, or transmission electron microscopy (TEM) to investigate their species-specific trophic interactions and potential symbiotic associations. 53–99% of 16S rRNA gene sequences recovered from two specimens of N. dutertrei were assigned to a single operational taxonomic unit (OTU) from a chloroplast of the phylum Stramenopile. TEM observations confirmed the presence of numerous intact coccoid algae within the host cell, consistent with algal symbionts. Based on sequence data and observed ultrastructure, we taxonomically assign the putative algal symbionts to Pelagophyceae and not Chrysophyceae, as previously reported in this species. In addition, our data shows that N. dutertrei feeds on protists within particulate organic matter (POM), but not on bacteria as a major food source. In total contrast, of OTUs recovered from three N. incompta specimens, 83–95% were assigned to bacterial classes Alteromonadales and Vibrionales of the order Gammaproteobacteria. TEM demonstrates that these bacteria are a food source, not putative symbionts. Contrary to the current view that non-spinose foraminifera are predominantly herbivorous, neither N. dutertrei nor N. incompta contained significant numbers of phytoplankton OTUs. We present an alternative view of their trophic interactions and discuss these results within the context of modelling global planktonic foraminiferal abundances in response to high-latitude climate change.Publisher PDFPeer reviewe

Optimizing LA-ICP-MS analytical procedures for elemental depth profiling of foraminifera shells

Laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) is becoming a widespread technique for analyzing elemental ratios in foraminiferal calcite. Here we focus on optimizing LA-ICP-MS for high-resolution depth profiling of elemental ratios through shell walls. This application reveals intrashell variability and provides a unique opportunity to quantify trace element incorporation over short time scales of calcification by an individual foraminifer. High-resolution depth profiling requires careful consideration of both ablation and analytical conditions required to resolve differences in shell chemistry across sub-micron shell thickness. We present laser ablation profiles of NIST SRM 610 standard glass data (in cps) and elemental/Ca ratios (in mmol/mol) from foraminiferal calcite obtained over a range of operating conditions using a Photon Machines 193nm UV excimer laser-ablation system, equipped with a dual-volume ANU HelEx chamber, coupled to an Agilent 7700x quadrupole ICP-MS. Different combinations of energy density, repetition rate, and mass spectrometer cycle time can yield varying elemental profiles. This variability can mimic and/or mask real intrashell trace element heterogeneity in foraminifer shells. At low (<3Hz) laser repetition rates, real intrashell element variation can be obscured depending on the laser energy, whereas using moderate (≥3Hz) laser repetition rates and/or a signal-smoothing device improves the accuracy and precision of intrashell trace element profiles. Shell material is ablated rapidly when using a 5Hz or greater repetition rate and an energy density of 3J/cm2 or greater, resulting in reduced spatial resolution

LAtools: A data analysis package for the reproducible reduction of LA-ICPMS data

Laser Ablation Inductively Coupled Plasma Mass Spectrometry (LA-ICPMS) is an increasingly popular analytical technique, that is able to provide spatially resolved, minimally destructive analyses of heterogeneous materials. The data produced by this technique are inherently complex, and require extensive processing and subjective expert interpretation to produce useful compositional data. At present, laboratories employ diverse protocols for data processing, and the reporting of these protocols is usually insufficient to allow data processing to be independently replicated, rendering the resulting data untraceable. Importantly, different expert users can obtain significantly different results from the same raw data using nominally identical processing workflows, depending on how ‘contaminants’ are identified and excluded, and which regions of signal are selected as representative of the composition of the sample. The irreproducibility of LA-ICPMS is a significant problem for the technique, but the complexity of the raw data has been a major hindrance to developing traceable data processing workflows. Here, we present LAtools – a free, open-source Python package for LA-ICPMS data processing designed with reproducibility at its core. The software performs basic data processing with similar efficacy to existing software, and brings a number of new data selection algorithms to facilitate reproducible reduction of LA-ICPMS data. We discuss the key advances of LAtools, and compare its output to trace metal analysis of marine CaCO3 (foraminifera) processed both manually and with Iolite, and to manually processed trace element data from zircon grains.This research was supported with funds from the UC Davis Department of Earth and Planetary Sciences, the Research School of Earth Sciences, ANU, as well as U.S. National Science Foundation awards to HJS (EAR-0946297 and OCE-1061676) and JF (OCE1261519), and Australian Research Council awards to SE (DP0990010 and DP110103158)