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Competition for iron drives phytopathogen control by natural rhizosphere microbiomes


Gu, Shaohua; Wei, Zhong; Shao, Zhengying; Friman, Ville-Petri; Cao, Kehao; Yang, Tianjie; Kramer, Jos; Wang, Xiaofang; Li, Mei; Mei, Xinlan; Xu, Yangchun; Shen, Qirong; Kümmerli, Rolf; Jousset, Alexandre (2020). Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nature Microbiology, 5(8):1002-1010.

Abstract

Plant pathogenic bacteria cause high crop and economic losses to human societies1-3. Infections by such pathogens are challenging to control as they often arise through complex interactions between plants, pathogens and the plant microbiome4,5. This natural ecosystem is rarely studied experimentally at the microbiome-wide scale, and consequently we poorly understand how taxonomic and functional microbiome composition and the resulting ecological interactions affect pathogen growth and disease outbreak. Here we combine DNA-based soil microbiome analysis with in vitro and in planta bioassays to show that competition for iron via secreted siderophore molecules is a good predictor of microbe-pathogen interactions and plant protection. We examined the ability of 2150 individual bacterial members of 80 rhizosphere microbiomes, covering all major phylogenetic lineages, to suppress the bacterium Ralstonia solanacearum, a global phytopathogen capable of infecting various crops6,7. We found that secreted siderophores altered microbiome-pathogen interactions from complete pathogen suppression to strong facilitation. Rhizosphere microbiome members with growth-inhibitory siderophores could often suppress the pathogen in vitro, in natural and greenhouse soils, and protect tomato plants from infection. Conversely, rhizosphere microbiome members with growth-promotive siderophores were often inferior in competition and facilitated plant infection by the pathogen. Because siderophores are a chemically diverse group of molecules with each siderophore type relying on a compatible receptor for iron uptake8-12, our results suggest that pathogen-suppressive microbiome members produce siderophores the pathogen cannot use. Altogether, our study establishes a causal mechanistic link between microbiome-level competition for iron and plant protection and opens promising avenues to use siderophore-mediated interactions as a tool for microbiome engineering and pathogen control.

Abstract

Plant pathogenic bacteria cause high crop and economic losses to human societies1-3. Infections by such pathogens are challenging to control as they often arise through complex interactions between plants, pathogens and the plant microbiome4,5. This natural ecosystem is rarely studied experimentally at the microbiome-wide scale, and consequently we poorly understand how taxonomic and functional microbiome composition and the resulting ecological interactions affect pathogen growth and disease outbreak. Here we combine DNA-based soil microbiome analysis with in vitro and in planta bioassays to show that competition for iron via secreted siderophore molecules is a good predictor of microbe-pathogen interactions and plant protection. We examined the ability of 2150 individual bacterial members of 80 rhizosphere microbiomes, covering all major phylogenetic lineages, to suppress the bacterium Ralstonia solanacearum, a global phytopathogen capable of infecting various crops6,7. We found that secreted siderophores altered microbiome-pathogen interactions from complete pathogen suppression to strong facilitation. Rhizosphere microbiome members with growth-inhibitory siderophores could often suppress the pathogen in vitro, in natural and greenhouse soils, and protect tomato plants from infection. Conversely, rhizosphere microbiome members with growth-promotive siderophores were often inferior in competition and facilitated plant infection by the pathogen. Because siderophores are a chemically diverse group of molecules with each siderophore type relying on a compatible receptor for iron uptake8-12, our results suggest that pathogen-suppressive microbiome members produce siderophores the pathogen cannot use. Altogether, our study establishes a causal mechanistic link between microbiome-level competition for iron and plant protection and opens promising avenues to use siderophore-mediated interactions as a tool for microbiome engineering and pathogen control.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Department of Quantitative Biomedicine
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Life Sciences > Microbiology
Life Sciences > Immunology
Life Sciences > Applied Microbiology and Biotechnology
Life Sciences > Genetics
Health Sciences > Microbiology (medical)
Life Sciences > Cell Biology
Language:English
Date:1 August 2020
Deposited On:23 Dec 2020 16:27
Last Modified:24 Dec 2020 21:01
Publisher:Nature Publishing Group
ISSN:2058-5276
OA Status:Closed
Publisher DOI:https://doi.org/10.1038/s41564-020-0719-8
PubMed ID:32393858

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