Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph

International audience Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material with entrained bacteria). However, the role of such foraminifera in the benthic food web remains understudied. Foraminifera feeding on methanotrophic bacteria, which are 1...

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Published in:Biogeosciences
Main Authors: Schmidt, Christiane, Geslin, Emmanuelle, Bernhard, Joan, Lekieffre, Charlotte, Svenning, Mette Marianne, Roberge, Helene, Schweizer, Magali, Panieri, Giuliana
Other Authors: Laboratoire de Planétologie et Géosciences - Angers (LPG-ANGERS), Laboratoire de Planétologie et Géosciences UMR_C 6112 (LPG), Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST), Nantes Université - pôle Sciences et technologie, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Sciences et technologie, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST), Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ), The Arctic University of Norway Tromsø, Norway (UiT), Leibniz Centre for Tropical Marine Research (ZMT), Woods Hole Oceanographic Institution (WHOI), Université Grenoble Alpes (UGA), Photosymbiose, Physiologie cellulaire et végétale (LPCV), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), Institut des Matériaux de Nantes Jean Rouxel (IMN), Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST), Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - Ecole Polytechnique de l'Université de Nantes (Nantes Univ - EPUN), French scientific programme MOPGA (Make our Planet Great Again)223259NORCRUST255250German Research Foundation (DFG)444059848
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2022
Subjects:
GAS
Online Access:https://hal.science/hal-03791806
https://hal.science/hal-03791806/document
https://hal.science/hal-03791806/file/bg-19-3897-2022.pdf
https://doi.org/10.5194/bg-19-3897-2022
id ftunimainelemans:oai:HAL:hal-03791806v1
record_format openpolar
institution Open Polar
collection Le Mans Université: Archives Ouvertes (HAL)
op_collection_id ftunimainelemans
language English
topic SEA BENTHIC FORAMINIFERA
DEEP-SEA
CARBON
DELTA-C-13
SEDIMENTS
BACTERIA
INGESTION
RIDGE
GAS
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
[SDV.AEN]Life Sciences [q-bio]/Food and Nutrition
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
spellingShingle SEA BENTHIC FORAMINIFERA
DEEP-SEA
CARBON
DELTA-C-13
SEDIMENTS
BACTERIA
INGESTION
RIDGE
GAS
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
[SDV.AEN]Life Sciences [q-bio]/Food and Nutrition
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan
Lekieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
topic_facet SEA BENTHIC FORAMINIFERA
DEEP-SEA
CARBON
DELTA-C-13
SEDIMENTS
BACTERIA
INGESTION
RIDGE
GAS
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
[SDV.AEN]Life Sciences [q-bio]/Food and Nutrition
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
description International audience Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material with entrained bacteria). However, the role of such foraminifera in the benthic food web remains understudied. Foraminifera feeding on methanotrophic bacteria, which are 13C-depleted, may cause negative cytoplasmic and/or calcitic δ13C values. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (20 h) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti and analysed N. labradorica cytology via transmission electron microscopy (TEM). We hypothesised that M. sedimenti would be visible post-experiment in degradation vacuoles, as evidenced by their ultrastructure. 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 apertural area after 20 h incubation revealed three putative methanotrophs, close to clay particles, based on bacterial ultrastructural characteristics. Furthermore, we noted the absence of bacterial endobionts in all examined N. labradorica but confirmed the presence of kleptoplasts, which were often partially degraded. In sum, we suggest that M. sedimenti can be consumed via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site.
author2 Laboratoire de Planétologie et Géosciences - Angers (LPG-ANGERS)
Laboratoire de Planétologie et Géosciences UMR_C 6112 (LPG)
Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST)
Nantes Université - pôle Sciences et technologie
Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Sciences et technologie
Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST)
Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)
The Arctic University of Norway Tromsø, Norway (UiT)
Leibniz Centre for Tropical Marine Research (ZMT)
Woods Hole Oceanographic Institution (WHOI)
Université Grenoble Alpes (UGA)
Photosymbiose
Physiologie cellulaire et végétale (LPCV)
Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG)
Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG)
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)
Institut des Matériaux de Nantes Jean Rouxel (IMN)
Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST)
Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - Ecole Polytechnique de l'Université de Nantes (Nantes Univ - EPUN)
French scientific programme MOPGA (Make our Planet Great Again)223259NORCRUST255250German Research Foundation (DFG)444059848
format Article in Journal/Newspaper
author Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan
Lekieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
author_facet Schmidt, Christiane
Geslin, Emmanuelle
Bernhard, Joan
Lekieffre, Charlotte
Svenning, Mette Marianne
Roberge, Helene
Schweizer, Magali
Panieri, Giuliana
author_sort Schmidt, Christiane
title Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
title_short Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
title_full Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
title_fullStr Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
title_full_unstemmed Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph
title_sort deposit-feeding of nonionellina labradorica (foraminifera) from an arctic methane seep site and possible association with a methanotroph
publisher HAL CCSD
publishDate 2022
url https://hal.science/hal-03791806
https://hal.science/hal-03791806/document
https://hal.science/hal-03791806/file/bg-19-3897-2022.pdf
https://doi.org/10.5194/bg-19-3897-2022
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 ISSN: 1726-4170
EISSN: 1726-4189
Biogeosciences
https://hal.science/hal-03791806
Biogeosciences, 2022, 19 (16), pp.3897-3909. ⟨10.5194/bg-19-3897-2022⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.5194/bg-19-3897-2022
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https://hal.science/hal-03791806
https://hal.science/hal-03791806/document
https://hal.science/hal-03791806/file/bg-19-3897-2022.pdf
doi:10.5194/bg-19-3897-2022
WOS: 000847363200001
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.5194/bg-19-3897-2022
container_title Biogeosciences
container_volume 19
container_issue 16
container_start_page 3897
op_container_end_page 3909
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spelling ftunimainelemans:oai:HAL:hal-03791806v1 2024-05-12T07:57:59+00:00 Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph Schmidt, Christiane Geslin, Emmanuelle Bernhard, Joan Lekieffre, Charlotte Svenning, Mette Marianne Roberge, Helene Schweizer, Magali Panieri, Giuliana Laboratoire de Planétologie et Géosciences - Angers (LPG-ANGERS) Laboratoire de Planétologie et Géosciences UMR_C 6112 (LPG) Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST) Nantes Université - pôle Sciences et technologie Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Sciences et technologie Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Le Mans Université (UM)-Université d'Angers (UA)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST) Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ) The Arctic University of Norway Tromsø, Norway (UiT) Leibniz Centre for Tropical Marine Research (ZMT) Woods Hole Oceanographic Institution (WHOI) Université Grenoble Alpes (UGA) Photosymbiose Physiologie cellulaire et végétale (LPCV) Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG) Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA) Institut des Matériaux de Nantes Jean Rouxel (IMN) Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST) Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - Ecole Polytechnique de l'Université de Nantes (Nantes Univ - EPUN) French scientific programme MOPGA (Make our Planet Great Again)223259NORCRUST255250German Research Foundation (DFG)444059848 2022 https://hal.science/hal-03791806 https://hal.science/hal-03791806/document https://hal.science/hal-03791806/file/bg-19-3897-2022.pdf https://doi.org/10.5194/bg-19-3897-2022 en eng HAL CCSD European Geosciences Union info:eu-repo/semantics/altIdentifier/doi/10.5194/bg-19-3897-2022 hal-03791806 https://hal.science/hal-03791806 https://hal.science/hal-03791806/document https://hal.science/hal-03791806/file/bg-19-3897-2022.pdf doi:10.5194/bg-19-3897-2022 WOS: 000847363200001 info:eu-repo/semantics/OpenAccess ISSN: 1726-4170 EISSN: 1726-4189 Biogeosciences https://hal.science/hal-03791806 Biogeosciences, 2022, 19 (16), pp.3897-3909. ⟨10.5194/bg-19-3897-2022⟩ SEA BENTHIC FORAMINIFERA DEEP-SEA CARBON DELTA-C-13 SEDIMENTS BACTERIA INGESTION RIDGE GAS [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology [SDV.AEN]Life Sciences [q-bio]/Food and Nutrition [SDV.EE.IEO]Life Sciences [q-bio]/Ecology environment/Symbiosis info:eu-repo/semantics/article Journal articles 2022 ftunimainelemans https://doi.org/10.5194/bg-19-3897-2022 2024-04-17T15:15:00Z International audience Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material with entrained bacteria). However, the role of such foraminifera in the benthic food web remains understudied. Foraminifera feeding on methanotrophic bacteria, which are 13C-depleted, may cause negative cytoplasmic and/or calcitic δ13C values. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (20 h) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti and analysed N. labradorica cytology via transmission electron microscopy (TEM). We hypothesised that M. sedimenti would be visible post-experiment in degradation vacuoles, as evidenced by their ultrastructure. 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 apertural area after 20 h incubation revealed three putative methanotrophs, close to clay particles, based on bacterial ultrastructural characteristics. Furthermore, we noted the absence of bacterial endobionts in all examined N. labradorica but confirmed the presence of kleptoplasts, which were often partially degraded. In sum, we suggest that M. sedimenti can be consumed via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site. Article in Journal/Newspaper arctic methane Arctic Barents Sea Foraminifera* Storfjordrenna Le Mans Université: Archives Ouvertes (HAL) Arctic Barents Sea Storfjordrenna ENVELOPE(17.000,17.000,76.000,76.000) Biogeosciences 19 16 3897 3909