Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of the salt marsh foundation plant Spartina alterniflora.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
29 Apr 2024
Historique:
received: 23 05 2023
accepted: 09 04 2024
medline: 30 4 2024
pubmed: 30 4 2024
entrez: 29 4 2024
Statut: epublish

Résumé

Heterotrophic activity, primarily driven by sulfate-reducing prokaryotes, has traditionally been linked to nitrogen fixation in the root zone of coastal marine plants, leaving the role of chemolithoautotrophy in this process unexplored. Here, we show that sulfur oxidation coupled to nitrogen fixation is a previously overlooked process providing nitrogen to coastal marine macrophytes. In this study, we recovered 239 metagenome-assembled genomes from a salt marsh dominated by the foundation plant Spartina alterniflora, including diazotrophic sulfate-reducing and sulfur-oxidizing bacteria. Abundant sulfur-oxidizing bacteria encode and highly express genes for carbon fixation (RuBisCO), nitrogen fixation (nifHDK) and sulfur oxidation (oxidative-dsrAB), especially in roots stressed by sulfidic and reduced sediment conditions. Stressed roots exhibited the highest rates of nitrogen fixation and expression level of sulfur oxidation and sulfate reduction genes. Close relatives of marine symbionts from the Candidatus Thiodiazotropha genus contributed ~30% and ~20% of all sulfur-oxidizing dsrA and nitrogen-fixing nifK transcripts in stressed roots, respectively. Based on these findings, we propose that the symbiosis between S. alterniflora and sulfur-oxidizing bacteria is key to ecosystem functioning of coastal salt marshes.

Identifiants

pubmed: 38684658
doi: 10.1038/s41467-024-47646-1
pii: 10.1038/s41467-024-47646-1
doi:

Substances chimiques

Sulfur 70FD1KFU70
Sulfates 0
Nitrogen N762921K75

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3607

Subventions

Organisme : United States Department of Commerce | National Oceanic and Atmospheric Administration (NOAA)
ID : NA18OAR4170084
Organisme : National Science Foundation (NSF)
ID : DEB 1754756

Informations de copyright

© 2024. The Author(s).

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Auteurs

J L Rolando (JL)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.

M Kolton (M)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.
French Associates Institute for Agriculture and Biotechnology of Drylands, Ben-Gurion University of the Negev, Beer Sheva, Israel.

T Song (T)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.

Y Liu (Y)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.
The Pennsylvania State University, Department of Civil & Environmental Engineering, University Park, PA, 16802, USA.

P Pinamang (P)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.

R Conrad (R)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.

J T Morris (JT)

Belle Baruch Institute for Marine & Coastal Sciences, University of South Carolina, Columbia, SC, 29201, USA.

K T Konstantinidis (KT)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA.
Georgia Institute of Technology, School of Civil and Environmental Engineering, Atlanta, GA, 30332, USA.

J E Kostka (JE)

Georgia Institute of Technology, School of Biological Sciences, Atlanta, GA, 30332, USA. joel.kostka@biology.gatech.edu.
Georgia Institute of Technology, School of Earth and Atmospheric Sciences, Atlanta, GA, 30332, USA. joel.kostka@biology.gatech.edu.
Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA, 30332, USA. joel.kostka@biology.gatech.edu.

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Classifications MeSH