Dataset Information

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 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.

SUBMITTER: Zilius M

PROVIDER: S-EPMC7435186 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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N<sub>2</sub> fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.

Zilius Mindaugas M Bonaglia Stefano S Broman Elias E Chiozzini Vitor Gonsalez VG Samuiloviene Aurelija A Nascimento Francisco J A FJA Cardini Ulisse U Bartoli Marco M

Scientific reports 20200818 1

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 ...[more]

PMID: 32811860

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Project description:Dinitrogen (N2) fixation is a crucial source of bioavailable nitrogen in carbon-dominated cold seep systems. Previous studies have shown that diazotrophy is not necessarily dependent on sulfate-dependent anaerobic oxidation of methane for energy, and diverse catabolism can fuel the high-energy-demanding process in sediments. However, it remains unclear whether diazotroph can obtain energy by sulfur oxidation in sulfur-rich cold seep water column. Here, field investigations and in situ experiments were conducted in Haima cold seep to examine the effects of diverse sources of dissolved organic matter (DOM) on N2 fixation, specifically containing sulfur, carbon, nitrogen, and phosphorus. We found that active N2 fixation occurred in the water column above the Haima cold seep, with the Dechloromonas genus dominating the diazotroph community as revealed by nifH gene using high-throughput sequencing. In situ experiments showed an increased rate of N2 fixation (1.15- to 12.70-fold compared to that in control group) and a greater relative abundance of the Dechloromonas genus following enrichment with sulfur-containing organic matter. Furthermore, metagenomic assembly and binning revealed that Dechloromonas sp. carried genes related to N2 fixation (nifDHK) and sulfur compound oxidation (fccAB and soxABCXYZ), implying that the genus potentially serves as a multifunctional mediator for N2 fixation and sulfur cycling. Our results provide new insights regarding potential coupling mechanism associated with sulfur-driven N2 fixation in methane- and sulfide-rich environments.ImportanceN2 fixation is an important source of biologically available in carbon-dominated cold seep systems as little nitrogen is released by hydrocarbon seepage, thereby promoting biological productivity and the degradation of non-nitrogenous organic matter. Cold seeps are rich in diverse sources of dissolved organic matter (DOM) derived from the sinking of photosynthetic products in euphotic layer and the release of chemosynthesis products on the seafloor. However, it remains unclear whether N2 fixation is coupled to the metabolic processes of DOM, as determined by e.g., carbon, nitrogen, phosphorus, and sulfur content, for energy acquisition in sulfur-rich cold seeps. In this study, diazotroph community structure and its response to DOM compositions were revealed. Moreover, the metagenomics analysis suggested that Dechloromonas genus plays a dominant role in potential coupling N2 fixation and sulfur oxidation. Our study highlighted that sulfur oxidation in deep-sea cold seeps may serve as an energy source to drive N2 fixation.

Dataset Information

N₂ fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.

Publications

N<sub>2</sub> fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.

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Dataset Information

N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.

Publications

N<sub>2</sub> fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets

N₂ fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont.