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.
On the basis of in situ NO { 3 microprofiles and chamber incubations complemented by laboratory-based assessments of anammox and denitrification we evaluate the nitrogen turnover of an ocean margin sediment at 1450-m water depth. In situ NO N 2 production was attributed to prokaryotic denitrification (59%), anammox (37%), and foraminifera-based denitrification (4%). Anammox thereby represented an important nutrient sink, but the N 2 production was dominated by denitrification. Despite the fact that NO { 3 stored inside foraminifera represented ,80% of the total benthic NO { 3 pool, the slow intracellular NO { 3 turnover that, on average, sustained foraminifera metabolism for 12-52 d, contributed only to a minor extent to the overall N 2 production. The microbial activity in the surface sediment is a net nutrient sink of ,1.1 mmol N m 22 d 21 , which aligns with many studies performed in coastal and shelf environments. Continental margin areas can act as significant N sinks and play an important role in regional N budgets.
We measured organic carbon uptake rates by deep-sea benthic foraminifera and studied differences among species, living depth, and seasons to investigate how these protists contribute to carbon consumption on the deep-sea floor. In situ feeding experiments using 13 C-labeled algae were carried out in the central part of Sagami Bay from 24 to 29 November 2001 and 1 to 12 April 2002. Our results indicate that carbon assimilation rates were higher in shallow infaunal species (Uvigerina akitaensis, Bulimina aculeata) and lower in intermediate (Textularia kattegatensis) and deep infaunal species (Chilostomella ovoidea). Some shallow and intermediate infaunal species showed higher carbon uptake in spring than in autumn. In total, benthic foraminifera assimilated C at 5.8 Ϯ 4.8 mg m Ϫ2 and 2.0 Ϯ 1.3 mg m Ϫ2 (in spring and in autumn, respectively) of labeled algae within 2 d, which was more than that by total metazoans (1.5 Ϯ 0.4 mg m Ϫ2 and 0.4 Ϯ 0.1 mg m Ϫ2 , respectively). Deep-sea benthic foraminifera rapidly ingest large amounts of carbon and may play an important role in carbon consumption on the deep-sea floor. Different responses to algal carbon among species may explain foraminiferal assemblages and shifts after environmental changes, such as seasonal pulses of organic matter supply.
Deep-sea sediments harbour a vast biosphere. Archaea—one of the three domains of life1—are prevalent in marine environments2, 3, 4, 5, and comprise a significant fraction of the biomass in marine sediments6. Archaeal membranes are well characterized, and are comprised of a glycerol backbone and a nonpolar isoprenoid chain. However, the ecology of sedimentary archaea remains elusive, because it is difficult to grow them in the laboratory. Here, we trace the fate of 13C-labelled glucose added to marine sediments in Sagami Bay, Japan, to determine the in situ mechanisms of membrane synthesis. Following the addition of labelled glucose to sediment samples collected in the region, we placed the cores on the sea floor and sampled them after 9 and 405 days. We found that the 13C was incorporated into the glycerol backbone of archaeal membranes; 13C was apparent after 9 days of incubation, but most pronounced after 405 days. However, the isoprenoid chain of the membranes remained unlabelled. On the basis of the differential uptake of 13C, we suggest that the glycerol unit is synthesized de novo, whereas the isoprenoid unit is synthesized from relic archaeal membranes and detritus, because of the prevalence of these compounds in marine sediments. We therefore suggest that some benthic archaea build their membranes by recycling sedimentary organic compounds
Benthic foraminiferal food sources were examined in the central part of Sagami Bay, Japan (water depth 1450 m) based on an in situ feeding experiment with 13 C-labeled food materials. In this study, 3 different 13 C-labeled food materials were used: the unicellular marine algae Dunaliella tertiolecta, the marine diatom Chaetoceros sociale, and the marine bacterium Vibrio alginolyticus. The first two are representatives of phytodetritus and the third of organic matter produced in the sediments. Each type of food material was injected into a series of in situ culture cores and incubated for up to 21 d. We observed that some benthic foraminiferal species selectively ingested 13 C-labeled algae from the sedimentary organic matter. On the other hand, benthic foraminifera ingested 13 C-labeled bacteria unselectively from sedimentary organic matter. Total benthic foraminifera assimilated 8.8 mg C m-2 d-1 of sedimentary organic matter without phytodetritus assimilation. Based on the assimilation rates estimated in this experiment, we recognized 3 types of feeding strategy among deep-sea benthic foraminifera in Sagami Bay. There are those that ingest (1) fresh phytodetritus selectively (phytophagous species: Uvigerina akitaensis, Bolivina spissa, Bolivina pacifica); (2) fresh phytodetritus selectively but sedimentary organic matter as well when phytodetritus is absent (seasonal-phytophagous species: Bulimina aculeata, Textularia kattegatensis, Globobulimina affinis); and (3) sedimentary organic matter at random (deposit feeders: Cyclammina cancellata, Chilostomella ovoidea). These different types of carbon utilization should be considered not only for understanding modern ecosystems on the deep-sea floor but also for paleoceanographic reconstructions using the abundance and distribution, or isotopic composition, of benthic foraminifera.
Hadal trench bottom (>6000 m below sea level) sediments harbor higher microbial cell abundance compared with adjacent abyssal plain sediments. This is supported by the accumulation of sedimentary organic matter (OM), facilitated by trench topography. However, the distribution of benthic microbes in different trench systems has not been well explored yet. Here, we carried out small subunit ribosomal RNA gene tag sequencing for 92 sediment subsamples of seven abyssal and seven hadal sediment cores collected from three trench regions in the northwest Pacific Ocean: the Japan, Izu-Ogasawara, and Mariana Trenches. Tag-sequencing analyses showed specific distribution patterns of several phyla associated with oxygen and nitrate. The community structure was distinct between abyssal and hadal sediments, following geographic locations and factors represented by sediment depth. Co-occurrence network revealed six potential prokaryotic consortia that covaried across regions. Our results further support that the OM cycle is driven by hadal currents and/or rapid burial shapes microbial community structures at trench bottom sites, in addition to vertical deposition from the surface ocean. Our trans-trench analysis highlights intra-and inter-trench distributions of microbial assemblages and geochemistry in surface seafloor sediments, providing novel insights into ultradeep-sea microbial ecology, one of the last frontiers on our planet.
Among eukaryotes, some benthic foraminiferal species have been reported to be capable of nitrate respiration, although little is known about their denitrification processes. In this study, we incubated the shallow-water benthic foraminifer Ammonia beccarii with isotopically labeled sodium nitrate (273%, 0%, or +73%) under oxic or anoxic conditions to investigate how nitrate is used in foraminiferal cells and whether those signatures remain in amino acids. The d 15 N values of amino acids from bulk cells incubated under anoxic conditions were correlated with those of nitrate in seawater and were enriched in 15 N by up to , 50% compared to the isotopic compositions in seawater. There was no such relationship or enrichment in the cases of organic matter in the calcite tests under oxic or anoxic conditions or bulk cells under oxic conditions, suggesting that benthic foraminifera take up ambient nitrate under anoxic conditions and use it for denitrification; the remaining 15 N-enriched intracellular nitrate pool is used for amino acid synthesis, probably by endosymbiotic microbes, as suggested by observation of the cellular ultrastructure. The degree of 15 N enrichment may depend on denitrification rates of the intracellular nitrate pool. Because the amino acids in the calcite test are synthesized by foraminifera, they were not enriched in 15 N, even under anoxic conditions. Thus, differences between amino acid d 15 N of bulk foraminiferal cells and organic matter in tests may serve as a proxy for denitrification in foraminiferal cells and microbial amino acid synthesis under oxygen-depleted conditions.
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.
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