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

Abstract

AbstractSymbiotic root microbiota are crucial for plant growth as they assist their hosts in nutrient acquisition. In the roots of coastal marine plants, heterotrophic activity in the rhizosphere by sulfate-reducing microorganisms has been linked to nitrogen fixation. In this study, we recovered 239 high-quality metagenome-assembled genomes (MAGs) from a salt marsh dominated by the foundation plantSpartina alterniflora, including diazotrophic sulfate-reducing and sulfur-oxidizing bacteria thriving in the root compartment. Here we show for the first time that highly-abundant sulfur-oxidizing bacteria in the roots of a coastal macrophyte encode and highly express genes for nitrogen fixation (nifHDK). Further, we leveraged aS. alterniflorabiomass gradient to gain a mechanistic understanding on how root-microbe interactions respond to abiotic stress from anoxia and elevated sulfide concentration. We observed that the roots of the stressedS. alternifloraphenotype exhibited the highest rates of nitrogen fixation and expression levels of both the oxidative and reductive forms of the dissimilatory sulfite reductase gene (dsrAB). Approximately 25% and 15% of all sulfur-oxidizing dsrA and nitrogen-fixing nifK transcripts, respectively, were associated with novel MAGs of theCandidatusThiodiazotropha genus in the roots of the stressedS. alternifloraphenotype. We conclude that the rapid cycling of sulfur in the dynamicS. alternifloraroot zone is coupled to nitrogen fixation during both reductive and oxidative sulfur reactions, and that theS. alterniflora–Ca.Thiodiazotropha symbiosis is an adaptive response to anoxic and sulfidic sediment conditions, whereby the plants benefit from reduced sulfide toxicity and potential nitrogen acquisition.