Takashi Toyofuku

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.

Microdistribution of Mg/Ca, Sr/Ca, and Ba/Ca ratios in Pulleniatina obliquiloculata test by using a NanoSIMS: Implication for the vital effect mechanism

The Mg/Ca ratio within foraminiferal calcareous tests (shells) is widely used to reconstruct past seawater temperature. However, recent studies reported that the organic components within a test affect the Mg/Ca distribution. In this study, we have measured the Mg/Ca, Sr/Ca, and Ba/Ca ratios within the planktonic foraminifera Pulleniatina obliquiloculata by using a NanoSIMS (secondary ion mass spectrometer (SIMS)), which has excellent spatial resolution (∼1 μm) and allows us to compare the distribution of chemical compositions with that of the organic components. Element compositions show banding distributions composed of alternately higher and lower values of those elemental ratios. The Mg/Ca ratios, previously considered to be mainly controlled by calcification temperature, show larger variations than the values expected from the seawater temperature at the habitat depth of P. obliquiloculata. Comparison of the elemental distribution with the test microstructure reveals that the bands of high Mg/Ca and Sr/Ca ratios correspond with layers of the organic components. Such coincidence suggests that the organic components strongly affect the Mg/Ca and Sr/Ca ratios within a test. In spite of the heterogeneous distribution, temperature estimated from the averaged Mg/Ca ratio within a test is consistent with seawater temperature at the habitat depth of P. obliquiloculata, indicating that whole Mg/Ca ratio of foraminiferal test may be useful as paleotemperature proxy. In contrast to the Mg/Ca ratio the heterogenity in Ba/Ca ratio, which previously has been considered to be mainly controlled by the ambient seawater composition, is not fully matched with the layers of the organic compositions. Although the organic components concentrate Ba, other unknown factors appear to also cause heterogenity in Ba incorporation.

Evidence of Global Chlorophyll d

Although analyses of chlorophyll d (Chl d)‐dominated oxygenic photosystems have been conducted since their discovery 12 years ago, Chl d distribution in the environment and quantitative importance for aquatic photosynthesis remain to be investigated. We analyzed the pigment compositions of surface sediments and detected Chl d and its derivatives from diverse aquatic environments. Our data show that the viable habitat for Chl d‐producing phototrophs extends across salinities of 0 to 50 practical salinity units and temperatures of 1� to 40�C, suggesting that Chl d production can be ubiquitously observed in aquatic environments that receive near-infrared light. The relative abundances of Chl d derivatives over that of Chl a derivatives in the studied samples are up to 4%, further suggesting that Chl d‐based photosynthesis plays a quantitatively important role in the aquatic photosynthesis.

Hadal disturbance in the Japan Trench induced by the 2011 Tohoku–Oki Earthquake

In situ video observations and sediment core samplings were performed at two hadal sites in the Japan Trench on July, 2011, four months after the Tohoku–Oki earthquake. Video recordings documented dense nepheloid layers extending ~30–50 m above the sea bed. At the trench axis, benthic macrofauna was absent and dead organisms along with turbid downslope current were observed. The top 31 cm of sediment in the trench axis revealed three recent depositions events characterized by elevated 137Cs levels and alternating sediment densities. At 4.9 km seaward from the trench axis, little deposition was observed but the surface sediment contained 134Cs from the Fukushima Dai–ichi nuclear disaster. We argue that diatom blooms observed by remote sensing facilitated rapid deposition of 134Cs to hadal environment and the aftershocks induced successive sediment disturbances and maintained dense nepheloid layers in the trench even four months after the mainshock.

Cytologic and Genetic Characteristics of Endobiotic Bacteria and Kleptoplasts of Virgulinella fragilis (Foraminifera)

The benthic foraminifer Virgulinella fragilis Grindell and Collen 1976 has multiple putative symbioses with both bacterial and kleptoplast endobionts, possibly aiding its survival in environments from dysoxia (5–45 μmol‐O2/L) to microxia (0–5 μmol‐O2/L) and in the dark. To clarify the origin and function of V. fragilis endobionts, we used genetic analyses and transmission electron microscope observations. Virgulinella fragilis retained δ‐proteobacteria concentrated at its cell periphery just beneath the cell membranes. Unlike another foraminifer Stainforthia spp., which retains many bacterial species, V. fragilis has a less variable bacterial community. This suggests that V. fragilis maintains a specific intracellular bacterial flora. Unlike the endobiotic bacteria, V. fragilis klepto‐plasts originated from various diatom species and are found in the interior cytoplasm. We found evidence of both retention and digestion of kleptoplasts, and of fragmentation of the kleptoplastid outer membrane that likely facilitates transport of kleptoplastid products to the host. Accumulations of mitochondria were observed encircling endobiotic bacteria. It is likely that the bacteria use host organic material for carbon oxidation. The mitochondria may use oxygen available around the δ‐proteobacteria and synthesize adenosine triphosphate, perhaps for sulfide oxidation.

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.

Monothalamous Soft-Shelled Foraminifera at an Abyssal Site in the North Pacific: A Preliminary Report

Soft-shelled monothalamous foraminifera, including species belonging to the suborders Allogromiida and Astrorhizida (families Saccamminidae and Psammosphaeridae), are an abundant and diverse component of the meiofauna in the deep NE Atlantic but have never been systematically documented in the Pacific Ocean. We examined the 32–63 µm and >63 µm fractions of a sample (0–1 cm layer, surface area 52.8 cm2) from an abyssal plain in the subarctic North Pacific, close to the Aleutian Trench (48°05.43′ N, 176°55.06′ E; 5289 m water depth). The residues yielded an estimated 2876 stained foraminifera (=545 per 10 cm2) of which >75% occurred in the upper 0.5 cm layer and almost half in the 32–63 µm fraction. Rather less than a third (30.5%) of individuals, and about half of the morphospecies (56 out of 121), were soft-shelled monothalamous forms. Many of these, particularly the saccamminids, were tiny, <120 µm in maximum dimension. Based on our analysis of this sample, and previous results in the North Atlantic and NW Indian Oceans, we suggest that these poorly known taxa are a consistently important component of the abyssal meiofauna in well-oxygenated areas.

Intracellular Isotope Localization in Ammonia sp. (Foraminifera) of Oxygen-Depleted Environments: Results of Nitrate and Sulfate Labeling Experiments

Some benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation with isotopically labeled nitrate and sulfate in dysoxic or anoxic conditions. After 2 weeks of incubation, foraminiferal specimens were fixed and prepared for Transmission Electron Microscopy (TEM) and correlative nanometer-scale secondary ion mass spectrometry (NanoSIMS) analyses. TEM observations revealed that there were characteristic ultrastructural features typically near the cell periphery in the youngest two or three chambers of the foraminifera exposed to anoxic conditions. These structures, which are electron dense and ~200–500 nm in diameter and co-occurred with possible endobionts, were labeled with 15N originated from 15N-labeled nitrate under anoxia and were labeled with both 15N and 34S under dysoxia. The labeling with 15N was more apparent in specimens from the dysoxic incubation, suggesting higher foraminiferal activity or increased availability of the label during exposure to oxygen depletion than to anoxia. Our results suggest that the electron dense bodies in Ammonia sp. play a significant role in nitrate incorporation and/or subsequent nitrogen assimilation during exposure to dysoxic to anoxic conditions.

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.

Deep-sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean

Whale carcasses create remarkable habitats in the deep-sea by producing concentrated sources of organic matter for a food-deprived biota as well as places of evolutionary novelty and biodiversity. Although many of the faunal patterns on whale falls have already been described, the biogeography of these communities is still poorly known especially from basins other than the NE Pacific Ocean. The present work describes the community composition of the deepest natural whale carcass described to date found at 4204 m depth on Southwest Atlantic Ocean with manned submersible Shinkai 6500. This is the first record of a natural whale fall in the deep Atlantic Ocean. The skeleton belonged to an Antarctic Minke whale composed of only nine caudal vertebrae, whose degradation state suggests it was on the bottom for 5–10 years. The fauna consisted mainly of galatheid crabs, a new species of the snail Rubyspira and polychaete worms, including a new Osedax species. Most of the 41 species found in the carcass are new to science, with several genera shared with NE Pacific whale falls and vent and seep ecosystems. This similarity suggests the whale-fall fauna is widespread and has dispersed in a stepping stone fashion, deeply influencing its evolutionary history.