Foraminiferal Ecology and Role in Nitrogen Benthic Cycle in the Hypoxic Southeastern Bering Sea

Abstract

Southeastern Bering Sea is one of the highest surface productivity area in the open ocean due to strong upwelling along the Bering canyon. However, the benthic geochemistry and organisms living in the area have been largely overlooked. In August 2017, surface sediment was sampled from four stations along a transect at depths between 1536 and 103 meters in the Bering canyon with JAMSTEC R/V Mirai. Bottom-water hypoxia was recorded in the two deepest stations (1536 and 536 m). At these stations, the oxygen penetrated down to 5 mm in the sediment due to siltier and much organic-rich sediments in the deeper stations while oxygen penetration was about 20 mm at stations 103 and 197 m deep with coarse-grained sediment stations. Foraminiferal number of species and abundances were higher in the Unimak pass depression station E2 (197 m). Abundance did not change significantly between stations, suggesting that foraminiferal densities are not affected by the hypoxic conditions but are rather controlled by organic matter and nutrients availability. At the upper bathyal and middle bathyal stations, living foraminiferal communities were in general dominated by Uvigerina peregrina, Nonionella pulchella, Elphidium batialis, Globobulimina pacifica, Reophax spp., and Bolivina spathulata while the shallower stations exhibited large densities of Uvigerina peregrina, Cibicidoides wuellerstorfi, Recurvoidella bradyi, Globocassidulina subglobosa, and Portatrochammina pacifica. More than 50% of the individuals have a potential to accumulate nitrate in their cell (from 3 to 648 mmol/L; which is from 100 to 4000 times larger than the highest concentration measured in pore water). Onboard denitrification measurements confirmed that B. spathulata, N. pulchella and G. pacifica could reduce nitrate through denitrification and foraminiferal denitrification could contribute over 6% to benthic nitrate reduction at the southeast Bering Sea. Although the foraminiferal contributions were smaller than those measured at other hypoxic areas, our study quantitatively revealed the significance of eukaryotic microbes on benthic nitrogen cycles at this area.

Single-celled bioturbators: benthic foraminifera mediate oxygen penetration and prokaryotic diversity in intertidal sediment

“…In our study, benthic foraminifera improved the pore-water oxygenation, and their burrows might also affect a series of diagenetic processes. Indeed, coastal foraminifera are known to accumulate large amounts of nitrate in their cells Langlet et al, 2014;LeKieffre et al, 2022) and deep-sea foraminifera can reduce nitrate and greatly contribute to benthic denitrification (Langlet et al, 2020;Choquel et al, 2021). Our results suggest that foraminiferal bioturbation also affected the benthic nitrogen cycle since lower total nitrogen (TN) content were measured in sediments bioturbated by foraminifera in comparison with non-bioturbated sediments.…”

Single-celled bioturbators: benthic foraminifera mediate oxygen penetration and prokaryotic diversity in intertidal sediment

“…In our study, benthic foraminifera improved the pore-water oxygenation, and their burrows might also affect a series of diagenetic processes. Indeed, coastal foraminifera are known to accumulate large amounts of nitrate in their cells (Geslin et al, 2014;Langlet et al, 2014;LeKieffre et al, 2022), and deep-sea foraminifera can reduce nitrate and greatly contribute to benthic denitrification (Langlet et al, 2020;Choquel et al, 2021). Our results suggest that foraminiferal bioturbation also affected the benthic nitrogen cycle via enhancing microbial OM degradation, since lower total nitrogen (TN) content was measured in sediments bioturbated by foraminifera in comparison with control sediments.…”

16S rRNA Gene Metabarcoding Indicates Species-Characteristic Microbiomes in Deep-Sea Benthic Foraminifera

“…Globobulimina pacifica is also a deep-infaunal species known to thrive in low-oxygen conditions (e.g., Corliss, 1985;Jorissen et al, 1995;Fontanier et al, 2002). This species can collect nitrate and denitrify (Table 2; Langlet et al, 2020). In previous studies, genus Globobulimina has been shown to perform complete denitrification itself (Woehle et al, 2018) and contain intracellular bacteria only in low abundance, suggesting a lack of bacterial endobionts (Risgaard-Petersen et al, 2006).…”

“…During the KM19-07 cruise in 2019, onboard analyses of a core (SB19; Table 1) for both dissolved pore water oxygen and nutrients (nitrite, nitrate, and ammonium) were carried out as described in Langlet et al (2020). In brief, oxygen micro-profiling was carried out in a cold room at 4°C immediately after sediment sampling.…”

“…Nitrate respiration rates were then determined based on Fick's first law of diffusion from steady-state N 2 O profiles measured with a N 2 O micro electrode (Andersen et al, 2001) after acetylene inhibition of N 2 O reduction (Smith et al, 1978;Risgaard-Petersen et al, 2006;Høgslund et al, 2008) in anoxic and nitrate free ASW at 11°C. Specimens selected for intracellular nitrate determination were placed in 1 ml centrifugation microtubes and frozen at −80°C to break the foraminiferal cell and conserve the samples until further nutrient content analysis by following Nomaki et al (2015) and Langlet et al (2020). Nitrate and nitrite extraction from the foraminiferal cells was achieved by freezing at −80°C, and the frozen cells were then dissolved in 200 μl of MilliQ water and homogenized in the microtube using a plastic pestle.…”