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

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 fixatio...

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Bibliographic Details
Published in:	Nature communications Vol. 15; no. 1; p. 3607
Main Authors:	Rolando, J. L., Kolton, M., Song, T., Liu, Y., Pinamang, P., Conrad, R., Morris, J. T., Konstantinidis, K. T., Kostka, J. E.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 29-04-2024 Nature Publishing Group Nature Portfolio
Subjects:	38/22 38/23 38/39 38/77 45 45/22 45/23 45/77 45/90 45/91 631/158/4016 631/326/171/1818 704/47/4112 Aquatic plants Bacteria Bacteria - classification Bacteria - genetics Bacteria - metabolism Carbon fixation Coastal ecosystems Coastal processes Ecological function Genes Genomes Humanities and Social Sciences Macrophytes Marine plants Metagenome Microbiomes multidisciplinary Nitrogen Nitrogen - metabolism Nitrogen Fixation Nitrogenation Oxidation Oxidation-Reduction Phylogeny Plant Roots - metabolism Plant Roots - microbiology Poaceae - metabolism Prokaryotes Ribulose-bisphosphate carboxylase Root zone Roots Salt marshes Science Science (multidisciplinary) Spartina alterniflora Sulfate reduction Sulfates Sulfates - metabolism Sulfur Sulfur - metabolism Sulfur oxidation Symbionts Symbiosis Wetlands
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Summary:	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. The mechanisms underlying plant-microbe interactions in coastal ecosystems are little explored. Here, the authors use multi-omics and biogeochemical measurements to investigate the saltmarsh cordgrass root microbiome and its role in coupling nitrogen fixation and sulfur cycling.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	2041-1723 2041-1723
DOI:	10.1038/s41467-024-47646-1