Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment

Choquel, Constance; Geslin, Emmanuelle; Metzger, Édouard; Filipsson, Helena L.; Risgaard-Petersen, Nils; Launeau, Patrick; Giraud, Manuel; Jauffrais, Thierry; Jesus, Bruno; Mouret, Aurélia

doi:10.5194/bg-18-327-2021

Cited by 27 publications

(46 citation statements)

References 79 publications

(116 reference statements)

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“…Benthic foraminifera have already been shown to be major contributors to the nitrogen cycle via their ability to denitrify (Risgaard-Petersen et al, 2006;Høgslund et al, 2008;Piña-Ochoa et al, 2010a;Bernhard et al, 2012;Glock et al, 2013;Glock et al, 2019;Choquel et al, 2021). However, not all foraminifera are able to denitrify, while our study shows ammonium assimilation in biomass for all the foraminiferal species investigated to date.…”

Section: Discussionmentioning

confidence: 43%

“…These organisms exhibit diverse life strategies, including heterotrophy, bacterial and/or algal symbioses, kleptoplasty (sequestered chloroplasts), anaerobic (nitrate) respiration, and dormancy (e.g., Goldstein, 1999;Nomaki et al, 2006;Jauffrais et al, 2016;Bernhard et al, 2018;Piña-Ochoa et al, 2010a;Ross and Hallock, 2016). This diversity of life strategies enables them to colonize a wide variety of benthic environments, where they are often considered substantial contributors to nitrogen biogeochemical cycling (Høgslund et al, 2008;Piña-Ochoa et al, 2010a;Glock et al, 2013;Choquel et al, 2021). The ability to denitrify (Risgaard-Petersen et al, 2006;Woehle et al, 2018;Gomaa et al, 2021) is widespread among foraminiferal species (Piña-Ochoa et al, 2010a) and represents a major metabolic pathway that can contribute up to 100% of the total denitrification in sediments (Choquel et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

“…This diversity of life strategies enables them to colonize a wide variety of benthic environments, where they are often considered substantial contributors to nitrogen biogeochemical cycling (Høgslund et al, 2008;Piña-Ochoa et al, 2010a;Glock et al, 2013;Choquel et al, 2021). The ability to denitrify (Risgaard-Petersen et al, 2006;Woehle et al, 2018;Gomaa et al, 2021) is widespread among foraminiferal species (Piña-Ochoa et al, 2010a) and represents a major metabolic pathway that can contribute up to 100% of the total denitrification in sediments (Choquel et al, 2021). Likely related to this, many benthic foraminifera are found to uptake and store nitrate intracellularly both in the presence and absence of oxygen (Piña-Ochoa et al, 2010b;Koho et al, 2011;Glock et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera

et al. 2022

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Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable 15N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding 15N and 34S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.

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Section: Discussionmentioning

confidence: 43%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera

et al. 2022

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“…stella (Risgaard-Petersen et al, 2006), and NIS Nonionella sp. T1 (Choquel et al, 2021), and has been speculated also for Nonionellina labradorica (reviewed (Charrieau et al, 2019).Next to its wide distribution, it is an especially interesting experimental species, because it hosts kleptoplasts, i.e. sequestered chloroplasts, of diatom origin inside its cytoplasm (Cedhagen, 1991;Jauffrais et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

Schmidt

Geslin²,

Bernhard

et al. 2021

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Abstract. Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material along with entrained bacteria). However, the role of such foraminifera in the benthic food-web remains understudied. As foraminifera may associate with methanotrophic bacteria, which are 13C-depleted, feeding on them has been suggested to cause negative δ13C values in the foraminiferal cytoplasm and/or calcite. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (1 d) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti, and analyzed N. labradorica cytology via Transmission Electron microscopy (TEM). We hypothesized that M. sedimenti would be visible, as evidenced by their ultrastructure, in degradation vacuoles after this feeding experiment. Sediment grains (mostly clay) occurred inside one or several degradation vacuoles in all foraminifers. In 24 % of the specimens from the feeding experiment degradation vacuoles also contained bacteria, although none could be confirmed to be the offered M. sedimenti. Observations of the area adjacent to the aperture after 20 h incubation revealed three putative methanotrophs, close to clay particles. These methanotrophs were identified based on internal characteristics such as a type I stacked intracytoplasmic membranes (ICM), storage granules (SG) and gram-negative cell walls (GNCW). Furthermore, N. labradorica specimens were examined for specific adaptations to this active Arctic methane-emission site; we noted the absence of bacterial endobionts in all specimens examined but confirmed the presence of kleptoplasts, which were often partially degraded. Based on these observations, we suggest that M. sedimenti can be consumed by N. labradorica via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site. These results suggest that if methanothrophs are available to the foraminifera in their habitat, their non-selective uptake could make a substantial contribution to altering δ13Ctest values. This in turn may impact metazoans grazing on benthic foraminifera by altering their δ13C signature.

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“…Foraminifera are widely distributed across the marine realm, where they can constitute large proportions of the benthos (1,2). This diverse protistan group is broadly implicated in biogeochemical cycling, where some foraminifera and/or their symbionts perform approximately 67-100% of total denitrification (3)(4)(5). Others are involved in sulfur cycling (6) and reactive oxygen species (ROS) chemistry (7).…”

Section: Introductionmentioning

confidence: 99%

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers

Gomaa

Billings

et al. 2022

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Certain benthic foraminifera are known to thrive in marine sediments with low oxygen or even without detectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain somewhat elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed that these two species utilize adaptable mitochondrial and peroxisomal metabolism that reflect their differing lifestyles. N. stella, most abundant in anoxia and characterized by the lack of food vacuoles and the abundance of intracellular lipid droplets, was predicted to couple the putative peroxisomal beta-oxidation and glyoxylate cycle with a versatile electron transport system and a partial TCA cycle running in the reductive direction. In contrast, B. argentea, most abundant in hypoxia and contains food vacuoles, was predicted to utilize the putative peroxisomal gluconeogenesis and a full TCA cycle but lacks the expression of key beta-oxidation and glyoxylate cycle genes. These metabolic adaptations likely confer ecological success while encountering deoxygenation and illuminate the importance of metabolic modifications and interactions between mitochondria and peroxisomes in protists.ImportanceForaminiferan protists are nearly ubiquitous in today’s oceans and likely were major components of the Neoproterozoic protistan community. While largely considered aerobic, certain foraminifera demonstrate surprising adaptability to hypoxia and anoxia, contributing to biogeochemical cycling in benthic environments. The analyses of Rhizarian adaptive metabolism set the stage for studying other microeukaryotes under increasing ocean deoxygenation. Revealing the metabolic roles of foraminifera in anaerobic biogeochemical cycling should spur reassessments of existing paleoecological datasets as well as new perspectives on the metabolic evolution of eukaryotic cells.

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Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment

Cited by 27 publications

References 79 publications

Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera

Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

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