N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont

Abstract Mangrove forests are among the most productive and diverse ecosystems on the planet, despite limited nitrogen (N) availability. Under such conditions, animal-microbe associations (holobionts) are often key to ecosystem functioning. Here, we investigated the role of fiddler crabs and their c...

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Autores principales: Mindaugas Zilius, Stefano Bonaglia, Elias Broman, Vitor Gonsalez Chiozzini, Aurelija Samuiloviene, Francisco J. A. Nascimento, Ulisse Cardini, Marco Bartoli
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Publicado: Nature Portfolio 2020
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Acceso en línea:https://doaj.org/article/fb67db95c4d043baae424f1939596b1f
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spelling oai:doaj.org-article:fb67db95c4d043baae424f1939596b1f2021-12-02T16:45:53ZN2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont10.1038/s41598-020-70834-02045-2322https://doaj.org/article/fb67db95c4d043baae424f1939596b1f2020-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-70834-0https://doaj.org/toc/2045-2322Abstract Mangrove forests are among the most productive and diverse ecosystems on the planet, despite limited nitrogen (N) availability. Under such conditions, animal-microbe associations (holobionts) are often key to ecosystem functioning. Here, we investigated the role of fiddler crabs and their carapace-associated microbial biofilm as hotspots of microbial N transformations and sources of N within the mangrove ecosystem. 16S rRNA gene and metagenomic sequencing provided evidence of a microbial biofilm dominated by Cyanobacteria, Alphaproteobacteria, Actinobacteria, and Bacteroidota with a community encoding both aerobic and anaerobic pathways of the N cycle. Dinitrogen (N2) fixation was among the most commonly predicted process. Net N fluxes between the biofilm-covered crabs and the water and microbial N transformation rates in suspended biofilm slurries portray these holobionts as a net N2 sink, with N2 fixation exceeding N losses, and as a significant source of ammonium and dissolved organic N to the surrounding environment. N stable isotope natural abundances of fiddler crab carapace-associated biofilms were within the range expected for fixed N, further suggesting active microbial N2 fixation. These results extend our knowledge on the diversity of invertebrate-microbe associations, and provide a clear example of how animal microbiota can mediate a plethora of essential biogeochemical processes in mangrove ecosystems.Mindaugas ZiliusStefano BonagliaElias BromanVitor Gonsalez ChiozziniAurelija SamuilovieneFrancisco J. A. NascimentoUlisse CardiniMarco BartoliNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-14 (2020)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Mindaugas Zilius
Stefano Bonaglia
Elias Broman
Vitor Gonsalez Chiozzini
Aurelija Samuiloviene
Francisco J. A. Nascimento
Ulisse Cardini
Marco Bartoli
N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
description Abstract Mangrove forests are among the most productive and diverse ecosystems on the planet, despite limited nitrogen (N) availability. Under such conditions, animal-microbe associations (holobionts) are often key to ecosystem functioning. Here, we investigated the role of fiddler crabs and their carapace-associated microbial biofilm as hotspots of microbial N transformations and sources of N within the mangrove ecosystem. 16S rRNA gene and metagenomic sequencing provided evidence of a microbial biofilm dominated by Cyanobacteria, Alphaproteobacteria, Actinobacteria, and Bacteroidota with a community encoding both aerobic and anaerobic pathways of the N cycle. Dinitrogen (N2) fixation was among the most commonly predicted process. Net N fluxes between the biofilm-covered crabs and the water and microbial N transformation rates in suspended biofilm slurries portray these holobionts as a net N2 sink, with N2 fixation exceeding N losses, and as a significant source of ammonium and dissolved organic N to the surrounding environment. N stable isotope natural abundances of fiddler crab carapace-associated biofilms were within the range expected for fixed N, further suggesting active microbial N2 fixation. These results extend our knowledge on the diversity of invertebrate-microbe associations, and provide a clear example of how animal microbiota can mediate a plethora of essential biogeochemical processes in mangrove ecosystems.
format article
author Mindaugas Zilius
Stefano Bonaglia
Elias Broman
Vitor Gonsalez Chiozzini
Aurelija Samuiloviene
Francisco J. A. Nascimento
Ulisse Cardini
Marco Bartoli
author_facet Mindaugas Zilius
Stefano Bonaglia
Elias Broman
Vitor Gonsalez Chiozzini
Aurelija Samuiloviene
Francisco J. A. Nascimento
Ulisse Cardini
Marco Bartoli
author_sort Mindaugas Zilius
title N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
title_short N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
title_full N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
title_fullStr N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
title_full_unstemmed N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
title_sort n2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont
publisher Nature Portfolio
publishDate 2020
url https://doaj.org/article/fb67db95c4d043baae424f1939596b1f
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