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

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 ca...

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Autores principales: Xu, Ling, Dong, Zhaobin, Chiniquy, Dawn, Pierroz, Grady, Deng, Siwen, Gao, Cheng, Diamond, Spencer, Simmons, Tuesday, Wipf, Heidi M.-L., Caddell, Daniel, Varoquaux, Nelle, Madera, Mary A., Hutmacher, Robert, Deutschbauer, Adam, Dahlberg, Jeffery A., Guerinot, Mary Lou, Purdom, Elizabeth, Banfield, Jillian F., Taylor, John W., Lemaux, Peggy G., Coleman-Derr, Devin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163885/
https://www.ncbi.nlm.nih.gov/pubmed/34050180
http://dx.doi.org/10.1038/s41467-021-23553-7
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author Xu, Ling
Dong, Zhaobin
Chiniquy, Dawn
Pierroz, Grady
Deng, Siwen
Gao, Cheng
Diamond, Spencer
Simmons, Tuesday
Wipf, Heidi M.-L.
Caddell, Daniel
Varoquaux, Nelle
Madera, Mary A.
Hutmacher, Robert
Deutschbauer, Adam
Dahlberg, Jeffery A.
Guerinot, Mary Lou
Purdom, Elizabeth
Banfield, Jillian F.
Taylor, John W.
Lemaux, Peggy G.
Coleman-Derr, Devin
author_facet Xu, Ling
Dong, Zhaobin
Chiniquy, Dawn
Pierroz, Grady
Deng, Siwen
Gao, Cheng
Diamond, Spencer
Simmons, Tuesday
Wipf, Heidi M.-L.
Caddell, Daniel
Varoquaux, Nelle
Madera, Mary A.
Hutmacher, Robert
Deutschbauer, Adam
Dahlberg, Jeffery A.
Guerinot, Mary Lou
Purdom, Elizabeth
Banfield, Jillian F.
Taylor, John W.
Lemaux, Peggy G.
Coleman-Derr, Devin
author_sort Xu, Ling
collection PubMed
description 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.
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spelling pubmed-81638852021-06-17 Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics Xu, Ling Dong, Zhaobin Chiniquy, Dawn Pierroz, Grady Deng, Siwen Gao, Cheng Diamond, Spencer Simmons, Tuesday Wipf, Heidi M.-L. Caddell, Daniel Varoquaux, Nelle Madera, Mary A. Hutmacher, Robert Deutschbauer, Adam Dahlberg, Jeffery A. Guerinot, Mary Lou Purdom, Elizabeth Banfield, Jillian F. Taylor, John W. Lemaux, Peggy G. Coleman-Derr, Devin Nat Commun Article 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. Nature Publishing Group UK 2021-05-28 /pmc/articles/PMC8163885/ /pubmed/34050180 http://dx.doi.org/10.1038/s41467-021-23553-7 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Xu, Ling
Dong, Zhaobin
Chiniquy, Dawn
Pierroz, Grady
Deng, Siwen
Gao, Cheng
Diamond, Spencer
Simmons, Tuesday
Wipf, Heidi M.-L.
Caddell, Daniel
Varoquaux, Nelle
Madera, Mary A.
Hutmacher, Robert
Deutschbauer, Adam
Dahlberg, Jeffery A.
Guerinot, Mary Lou
Purdom, Elizabeth
Banfield, Jillian F.
Taylor, John W.
Lemaux, Peggy G.
Coleman-Derr, Devin
Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title_full Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title_fullStr Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title_full_unstemmed Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title_short Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
title_sort genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8163885/
https://www.ncbi.nlm.nih.gov/pubmed/34050180
http://dx.doi.org/10.1038/s41467-021-23553-7
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