Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics

Abstract

Recent studies have demonstrated that drought leads to dramatic, highly conserved shifts in the root microbiome. At present, the molecular mechanisms underlying these responses remain largely uncharacterized. Here we employ genome-resolved metagenomics and comparative genomics to demonstrate that carbohydrate and secondary metabolite transport functionalities are overrepresented within drought-enriched taxa. These data also reveal that bacterial iron transport and metabolism functionality is highly correlated with drought enrichment. Using time-series root RNA-Seq data, we demonstrate that iron homeostasis within the root is impacted by drought stress, and that loss of a plant phytosiderophore iron transporter impacts microbial community composition, leading to significant increases in the drought-enriched lineage, Actinobacteria. Finally, we show that exogenous application of iron disrupts the drought-induced enrichment of Actinobacteria, as well as their improvement in host phenotype during drought stress. Collectively, our findings implicate iron metabolism in the root microbiome’s response to drought and may inform efforts to improve plant drought tolerance to increase food security.

Rhizosphere microbiome: Functional compensatory assembly for plant fitness

“…Drought is one of the most common environmental stresses. A coupled study of genome-resolved metagenomics and comparative genomics demonstrated that bacterial iron transport and metabolism functionality in the sorghum rhizosphere are highly correlated with their enrichment under drought stress [60] . Specifically, drought stress induced the loss of a phytosiderophore iron transporter and consequently led to the enrichment of Actinobacteria, while this enrichment could be disrupted by the exogenous application of iron.…”

Root and Rhizosphere Processes under Drought: Digging Deeper to Enhance Ecosystem Resilience

“…He also advocates that harnessing the microbiome for modern agriculture may be fostered by integrating a multi‐Omics approach, advanced ecological theory, and modern informatics technology. Finally, using the EPICON project (https://phytozome-next.jgi.doe.gov/epicon/) as an example, he highlighted their progress on understanding the response of the sorghum microbiome to the drought that has emerged from collaboratively investigating the fungal mycobiome, the bacterial microbiome, the meta‐genome and meta‐transcriptome, and the host sorghum transcriptome and metabolome (Xu et al 2018, 2021 a , b , Gao et al 2019, 2020, 2022, Zhou et al 2020).…”

Raman-Deuterium Isotope Probing and Metagenomics Reveal the Drought Tolerance of the Soil Microbiome and Its Promotion of Plant Growth

“…While this culture-based approach is suitable for studying symbiosis between a single bacterial species and a plant, its ability to systematically evaluate the drought tolerance of a highly diverse soil microbiome is limited. Metagenomic approaches have confirmed that the abundances of various strains belonging to classes Alpha- , Beta- , and Gammaproteobacteria , Actinobacteria , Bacilli , and Planctomycetia increase rapidly under drought stress ( 2 , 10 , 11 ). In addition to the drought survival strategies mentioned above, expression levels of genes associated with various metabolic processes such as osmolyte accumulation, biofilm formation, antioxidant molecule synthesis, and phytohormone synthesis have also been demonstrated to increase in DTB ( 12 ).…”

“…Drought can change plant phenotypes as well as symbiotic microbiomes, either directly or indirectly. The reduction of soil moisture and the restriction of access to nutrients can both directly affect soil microbiome diversity and compositional changes ( 2 ). These influences also affect the soil microbiome; they can change the composition and volume of root exudates containing sugars, amino acids, and phytohormones, which are altered by stress-induced phenotypes ( 3 ).…”