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

Author

Listed:
  • Ling Xu

    (University of California
    China Agricultural University)

  • Zhaobin Dong

    (University of California)

  • Dawn Chiniquy

    (Lawrence Berkeley National Laboratory)

  • Grady Pierroz

    (University of California)

  • Siwen Deng

    (University of California)

  • Cheng Gao

    (University of California)

  • Spencer Diamond

    (University of California)

  • Tuesday Simmons

    (University of California)

  • Heidi M.-L. Wipf

    (University of California)

  • Daniel Caddell

    (Plant Gene Expression Center, USDA-ARS)

  • Nelle Varoquaux

    (CNRS, University Grenoble Alpes, TIMC-IMAG)

  • Mary A. Madera

    (University of California)

  • Robert Hutmacher

    (University of California)

  • Adam Deutschbauer

    (Lawrence Berkeley National Laboratory)

  • Jeffery A. Dahlberg

    (Kearney Agricultural Research & Extension Center)

  • Mary Lou Guerinot

    (Dartmouth College)

  • Elizabeth Purdom

    (University of California)

  • Jillian F. Banfield

    (University of California)

  • John W. Taylor

    (University of California)

  • Peggy G. Lemaux

    (University of California)

  • Devin Coleman-Derr

    (University of California
    Plant Gene Expression Center, USDA-ARS)

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.

Suggested Citation

  • Ling Xu & Zhaobin Dong & Dawn Chiniquy & Grady Pierroz & Siwen Deng & Cheng Gao & Spencer Diamond & Tuesday Simmons & Heidi M.-L. Wipf & Daniel Caddell & Nelle Varoquaux & Mary A. Madera & Robert Hutm, 2021. "Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23553-7
    DOI: 10.1038/s41467-021-23553-7
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    Cited by:

    1. Ben O. Oyserman & Stalin Sarango Flores & Thom Griffioen & Xinya Pan & Elmar Wijk & Lotte Pronk & Wouter Lokhorst & Azkia Nurfikari & Joseph N. Paulson & Mercedeh Movassagh & Nejc Stopnisek & Anne Kup, 2022. "Disentangling the genetic basis of rhizosphere microbiome assembly in tomato," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Sara M. Amolegbe & Adeline R. Lopez & Maria L. Velasco & Danielle J. Carlin & Michelle L. Heacock & Heather F. Henry & Brittany A. Trottier & William A. Suk, 2022. "Adapting to Climate Change: Leveraging Systems-Focused Multidisciplinary Research to Promote Resilience," IJERPH, MDPI, vol. 19(22), pages 1-18, November.
    3. Yanfen Zheng & Xuwen Cao & Yanan Zhou & Siqi Ma & Youqiang Wang & Zhe Li & Donglin Zhao & Yanzhe Yang & Han Zhang & Chen Meng & Zhihong Xie & Xiaona Sui & Kangwen Xu & Yiqiang Li & Cheng-Sheng Zhang, 2024. "Purines enrich root-associated Pseudomonas and improve wild soybean growth under salt stress," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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