Competition for iron drives phytopathogen control by natural rhizosphere microbiomes
- 10 May 2020
- journal article
- research article
- Published by Springer Science and Business Media LLC in Nature Microbiology
- Vol. 5 (8), 1002-+
- https://doi.org/10.1038/s41564-020-0719-8
Abstract
Plant pathogenic bacteria cause high crop and economic losses to human societies(1-3). Infections by such pathogens are challenging to control as they often arise through complex interactions between plants, pathogens and the plant microbiome(4,5). Experimental studies of this natural ecosystem at the microbiome-wide scale are rare, and consequently we have a poor understanding of how the 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 2,150 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 crops(6,7). 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 as well as 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 uptake(8-12), our results suggest that pathogen-suppressive microbiome members produce siderophores that the pathogen cannot use. 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. In rhizosphere microbial communities, iron competition via secreted siderophores can be used as a predictor of commensal-pathogen interactions and plant protection against infection with the pathogen Ralstonia solanacearum.This publication has 59 references indexed in Scilit:
- Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populationsProceedings of the National Academy of Sciences of the United States of America, 2012
- Emerging fungal threats to animal, plant and ecosystem healthNature, 2012
- UCHIME improves sensitivity and speed of chimera detectionBioinformatics, 2011
- Significant Association between Sulfate-Reducing Bacteria and Uranium-Reducing Microbial Communities as Revealed by a Combined Massively Parallel Sequencing-Indicator Species ApproachApplied and Environmental Microbiology, 2010
- QIIME allows analysis of high-throughput community sequencing dataNature Methods, 2010
- Bacterial competition: surviving and thriving in the microbial jungleNature Reviews Microbiology, 2009
- Siderophore-Based Iron Acquisition and Pathogen ControlMicrobiology and Molecular Biology Reviews, 2007
- Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology driversTrends in Ecology & Evolution, 2004
- Bacterial iron homeostasisFEMS Microbiology Reviews, 2003
- The Ecology and Biogeography of Microorganisms on Plant SurfacesAnnual Review of Phytopathology, 2000