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

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 13 C-de...

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Main Authors: Schmidt, Christiane, Geslin, Emmanuelle, Bernhard, Joan M., LeKieffre, Charlotte, Svenning, Mette Marianne, Roberge, Helene, Schweizer, Magali, Panieri, Giuliana
Format: Text
Language:English
Published: 2021
Subjects:
Online Access:https://doi.org/10.5194/bg-2021-284
https://bg.copernicus.org/preprints/bg-2021-284/
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spelling ftcopernicus:oai:publications.copernicus.org:bgd98656 2023-05-15T14:31:45+02:00 Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy Schmidt, Christiane Geslin, Emmanuelle Bernhard, Joan M. LeKieffre, Charlotte Svenning, Mette Marianne Roberge, Helene Schweizer, Magali Panieri, Giuliana 2021-11-10 application/pdf https://doi.org/10.5194/bg-2021-284 https://bg.copernicus.org/preprints/bg-2021-284/ eng eng doi:10.5194/bg-2021-284 https://bg.copernicus.org/preprints/bg-2021-284/ eISSN: 1726-4189 Text 2021 ftcopernicus https://doi.org/10.5194/bg-2021-284 2021-11-15T17:22:28Z 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 13 C-depleted, feeding on them has been suggested to cause negative δ 13 C 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 δ 13 C test values. This in turn may impact metazoans grazing on benthic foraminifera by altering their δ 13 C signature. Text arctic methane Arctic Barents Sea Foraminifera* Storfjordrenna Copernicus Publications: E-Journals Arctic Barents Sea Storfjordrenna ENVELOPE(17.000,17.000,76.000,76.000)
institution Open Polar
collection Copernicus Publications: E-Journals
op_collection_id ftcopernicus
language English
description 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 13 C-depleted, feeding on them has been suggested to cause negative δ 13 C 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 δ 13 C test values. This in turn may impact metazoans grazing on benthic foraminifera by altering their δ 13 C signature.
format Text
author Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan M.
LeKieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
spellingShingle Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan M.
LeKieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
author_facet Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan M.
LeKieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
author_sort Schmidt, Christiane
title Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
title_short Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
title_full Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
title_fullStr Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
title_full_unstemmed Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
title_sort deposit feeding of a foraminifera from an arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy
publishDate 2021
url https://doi.org/10.5194/bg-2021-284
https://bg.copernicus.org/preprints/bg-2021-284/
long_lat ENVELOPE(17.000,17.000,76.000,76.000)
geographic Arctic
Barents Sea
Storfjordrenna
geographic_facet Arctic
Barents Sea
Storfjordrenna
genre arctic methane
Arctic
Barents Sea
Foraminifera*
Storfjordrenna
genre_facet arctic methane
Arctic
Barents Sea
Foraminifera*
Storfjordrenna
op_source eISSN: 1726-4189
op_relation doi:10.5194/bg-2021-284
https://bg.copernicus.org/preprints/bg-2021-284/
op_doi https://doi.org/10.5194/bg-2021-284
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