TY - JOUR
T1 - Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
AU - Xu, Ling
AU - Dong, Zhaobin
AU - Chiniquy, Dawn
AU - Pierroz, Grady
AU - Deng, Siwen
AU - Gao, Cheng
AU - Diamond, Spencer
AU - Simmons, Tuesday
AU - Wipf, Heidi M.L.
AU - Caddell, Daniel
AU - Varoquaux, Nelle
AU - Madera, Mary A.
AU - Hutmacher, Robert
AU - Deutschbauer, Adam
AU - Dahlberg, Jeffery A.
AU - Guerinot, Mary Lou
AU - Purdom, Elizabeth
AU - Banfield, Jillian F.
AU - Taylor, John W.
AU - Lemaux, Peggy G.
AU - Coleman-Derr, Devin
N1 - Funding Information:
We thank Feng Yu for participating in the sample collection, tissue grinding, DNA extraction, and providing thoughtful suggestions. We thank Nabila Riaz’s help with analysis of iron-regulated gene expression. We thank Bailey Bonnet for sharing microbial technology. We thank Alex Styer for helping with sample collection and sharing his R color palette. We thank Joy Hollingsworth and Julie A Sievert for participating in the sample collection. We thank Matthew Traxler and Bridget Hansen for discussing the project. This work was funded by the Department of Energy Grant DE-SC0014081. This work was also funded by National Institutes of Health grant P42 ES007373 to M. L. G.
Publisher Copyright:
© 2021, This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
PY - 2021/5/28
Y1 - 2021/5/28
N2 - 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.
AB - 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.
UR - https://www.scopus.com/pages/publications/85107008998
U2 - 10.1038/s41467-021-23553-7
DO - 10.1038/s41467-021-23553-7
M3 - Article
C2 - 34050180
AN - SCOPUS:85107008998
SN - 2041-1723
VL - 12
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 3209
ER -