Partitioning benthic nitrogen cycle processes among three common macrofauna holobionts

The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (nor...

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Published in:Biogeochemistry Vol. 157; no. 2; pp. 193 - 213
Main Authors: Zilius, Mindaugas, Daunys, Darius, Bartoli, Marco, Marzocchi, Ugo, Bonaglia, Stefano, Cardini, Ulisse, Castaldelli, Giuseppe
Format: Journal Article
Language:English
Published: Cham Springer International Publishing 2022
Springer Nature B.V
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Abstract The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (northern Baltic Sea). Solute fluxes and N transformations (N 2 fixation, denitrification and dissimilative nitrate reduction to ammonium [DNRA]) were measured in sediments and macrofauna-associated microbes (holobionts) to partition the role of three dominant taxa (the filter feeder Limecola balthica , the deep deposit feeder Marenzelleria spp., and the surface deposit feeder Monoporeia affinis ) in shaping N-cycling. In the studied area, benthic macrofauna comprised a low diversity community with dominance of the three taxa, which are widespread and dominant in the Baltic. The biomass of these taxa in macrofaunal community explained up to 30% of variation in measured biogeochemical processes, confirming their important role in ecosystem functioning. The results also show that these taxa significantly contributed to the benthic metabolism and N-cycling (direct effect) as well as to sediments bioturbation with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a reuse of nutrients at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in macrofauna holobionts suggested a community-associated versatile microbiome, however, its role was of minor importance as compared to the activity of sediment-associated microbial communities. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered analysing benthic functioning.
AbstractList The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (northern Baltic Sea). Solute fluxes and N transformations (N2 fixation, denitrification and dissimilative nitrate reduction to ammonium [DNRA]) were measured in sediments and macrofauna-associated microbes (holobionts) to partition the role of three dominant taxa (the filter feeder Limecola balthica, the deep deposit feeder Marenzelleria spp., and the surface deposit feeder Monoporeia affinis) in shaping N-cycling. In the studied area, benthic macrofauna comprised a low diversity community with dominance of the three taxa, which are widespread and dominant in the Baltic. The biomass of these taxa in macrofaunal community explained up to 30% of variation in measured biogeochemical processes, confirming their important role in ecosystem functioning. The results also show that these taxa significantly contributed to the benthic metabolism and N-cycling (direct effect) as well as to sediments bioturbation with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a reuse of nutrients at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in macrofauna holobionts suggested a community-associated versatile microbiome, however, its role was of minor importance as compared to the activity of sediment-associated microbial communities. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered analysing benthic functioning.
The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (northern Baltic Sea). Solute fluxes and N transformations (N 2 fixation, denitrification and dissimilative nitrate reduction to ammonium [DNRA]) were measured in sediments and macrofauna-associated microbes (holobionts) to partition the role of three dominant taxa (the filter feeder Limecola balthica , the deep deposit feeder Marenzelleria spp., and the surface deposit feeder Monoporeia affinis ) in shaping N-cycling. In the studied area, benthic macrofauna comprised a low diversity community with dominance of the three taxa, which are widespread and dominant in the Baltic. The biomass of these taxa in macrofaunal community explained up to 30% of variation in measured biogeochemical processes, confirming their important role in ecosystem functioning. The results also show that these taxa significantly contributed to the benthic metabolism and N-cycling (direct effect) as well as to sediments bioturbation with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a reuse of nutrients at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in macrofauna holobionts suggested a community-associated versatile microbiome, however, its role was of minor importance as compared to the activity of sediment-associated microbial communities. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered analysing benthic functioning.
Author Cardini, Ulisse
Bartoli, Marco
Zilius, Mindaugas
Castaldelli, Giuseppe
Bonaglia, Stefano
Marzocchi, Ugo
Daunys, Darius
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  surname: Zilius
  fullname: Zilius, Mindaugas
  email: mindaugas.zilius@jmtc.ku.lt
  organization: Marine Research Institute, Klaipeda University, Department of Life Science and Biotechnology, Ferrara University
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  fullname: Daunys, Darius
  organization: Marine Research Institute, Klaipeda University
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  surname: Bartoli
  fullname: Bartoli, Marco
  organization: Marine Research Institute, Klaipeda University, Department of Chemistry, Life Science and Environmental Sustainability, Parma University
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  givenname: Ugo
  surname: Marzocchi
  fullname: Marzocchi, Ugo
  organization: Marine Research Institute, Klaipeda University, Section for Microbiology, Department of Biology, Center for Electromicrobiology, Aarhus University, Department of Biology, Center for Water Technology (WATEC), Aarhus University
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  surname: Cardini
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  organization: Marine Research Institute, Klaipeda University, Integrative Marine Ecology Department, Stazione Zoologica Anton Dohrn, National Institute of Marine Biology, Ecology and Biotechnology
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  givenname: Giuseppe
  surname: Castaldelli
  fullname: Castaldelli, Giuseppe
  organization: Department of Life Science and Biotechnology, Ferrara University
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Keywords Nitrogen cycle
Benthic functioning
Sediments
Invertebrate-microbe associations
Nitrate reduction
Baltic Sea
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– name: Springer Nature B.V
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Snippet The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related...
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SubjectTerms Ammonium
Ammonium compounds
Annan geovetenskap och miljövetenskap
Baltic Sea
Benthic functioning
Benthos
Biogeosciences
Bioturbation
Bottom water
Cycles
Denitrification
Earth and Environmental Science
Earth Sciences
Ecological function
Ecology
Ecosystems
Ekologi
Environmental Chemistry
Estuaries
Estuarine dynamics
Filter feeders
Geochemistry
Geokemi
Geologi
Geology
Invertebrate-microbe associations
Life Sciences
Macrofauna
Marine crustaceans
Metabolism
Microbial activity
Microbiomes
Microorganisms
Nitrate reduction
Nitrogen
Nitrogen cycle
Nitrogen fixation
Nitrogenation
Nutrients
Other Earth and Related Environmental Sciences
Positive feedback
Reduction
Sediment
Sediments
Solutes
Zoobenthos
Zoologi
Zoology
Title Partitioning benthic nitrogen cycle processes among three common macrofauna holobionts
URI https://link.springer.com/article/10.1007/s10533-021-00867-8
https://www.proquest.com/docview/2619577907
https://gup.ub.gu.se/publication/309075
Volume 157
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