Dataset Information

Competition for iron drives phytopathogen control by natural rhizosphere microbiomes.

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.

SUBMITTER: Gu S

PROVIDER: S-EPMC7116525 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:Coffee is one of the most important commodities in the global market. Of the 130 species of Coffea, only Coffea arabica and Coffea canephora are actually cultivated on a large scale. Despite the economic and social importance of coffee, little research has been done on the coffee tree microbiome. To assess the structure and function of the rhizosphere microbiome, we performed a deep shotgun metagenomic sequencing of the rhizospheres of five different species, C. arabica, C. canephora, Coffea stenophylla, Coffea racemosa, and Coffea liberica. Our findings indicated that C. arabica and C. stenophylla have different microbiomes, while no differences were detected between the other Coffea species. The core rhizosphere microbiome comprises genera such as Streptomyces, Mycobacterium, Bradyrhizobium, Burkholderia, Sphingomonas, Penicillium, Trichoderma, and Rhizophagus, several of which are potential plant-beneficial microbes. Streptomyces and mycorrhizal fungi dominate the microbial communities. The concentration of sucrose in the rhizosphere seems to influence fungal communities, and the concentration of caffeine/theobromine has little effect on the microbiome. We also detected a possible relationship between drought tolerance in Coffea and known growth-promoting microorganisms. The results provide important information to guide future studies of the coffee tree microbiome to improve plant production and health. IMPORTANCE The microbiome has been identified as a fundamental factor for the maintenance of plant health, helping plants to fight diseases and the deleterious effects of abiotic stresses. Despite this, in-depth studies of the microbiome have been limited to a few species, generally with a short life cycle, and perennial species have mostly been neglected. The coffee tree microbiome, on the other hand, has gained interest in recent years as Coffea trees are perennial tropical species of enormous importance, especially for developing countries. A better understanding of the microorganisms associated with coffee trees can help to mitigate the deleterious effects of climate change on the crop, improving plant health and making the system more sustainable.

Project description:Disease-suppressive soils protect plants against soilborne fungal pathogens that would otherwise cause root infections. Soil suppressiveness is, in most cases, mediated by the antagonistic activity of the microbial community associated with the plant roots. Considering the enormous taxonomic and functional diversity of the root-associated microbiome, identification of the microbial genera and mechanisms underlying this phenotype is challenging. One approach to unravel the underlying mechanisms is to identify metabolic pathways enriched in the disease-suppressive microbial community, in particular, pathways that harbor natural products with antifungal properties. An important class of these natural products includes peptides produced by nonribosomal peptide synthetases (NRPSs). Here, we applied functional amplicon sequencing of NRPS-associated adenylation domains (A domains) to a collection of eight soils that are suppressive or nonsuppressive (i.e., conducive) to Fusarium culmorum, a fungal root pathogen of wheat. To identify functional elements in the root-associated bacterial community, we developed an open-source pipeline, referred to as dom2BGC, for amplicon annotation and putative gene cluster reconstruction through analyzing A domain co-occurrence across samples. We applied this pipeline to rhizosphere communities from four disease-suppressive and four conducive soils and found significant similarities in NRPS repertoires between suppressive soils. Specifically, several siderophore biosynthetic gene clusters were consistently associated with suppressive soils, hinting at competition for iron as a potential mechanism of suppression. Finally, to validate dom2BGC and to allow more unbiased functional metagenomics, we performed 10× metagenomic sequencing of one suppressive soil, leading to the identification of multiple gene clusters potentially associated with the disease-suppressive phenotype. IMPORTANCE Soil-borne plant-pathogenic fungi continue to be a major threat to agriculture and horticulture. The genus Fusarium in particular is one of the most devastating groups of soilborne fungal pathogens for a wide range of crops. Our approach to develop novel sustainable strategies to control this fungal root pathogen is to explore and exploit an effective, yet poorly understood naturally occurring protection, i.e., disease-suppressive soils. After screening 28 agricultural soils, we recently identified four soils that were suppressive to root disease of wheat caused by Fusarium culmorum. We also confirmed, via sterilization and transplantation, that the microbiomes of these soils play a significant role in the suppressive phenotype. By adopting nonribosomal peptide synthetase (NRPS) functional amplicon screening of suppressive and conducive soils, we here show how computationally driven comparative analysis of combined functional amplicon and metagenomic data can unravel putative mechanisms underlying microbiome-associated plant phenotypes.

Project description:BackgroundStudies on the rhizosphere microbiome of various plants proved that rhizosphere microbiota carries out various vital functions and can regulate the growth and improve the yield of plants. However, the rhizosphere microbiome of commercial blueberry was only reported by a few studies and remains elusive. Comparison and interpretation of the characteristics of the rhizosphere microbiome of blueberry are critical important to maintain its health.ResultsIn this study, a total of 20 rhizosphere soil samples, including 15 rhizosphere soil samples from three different blueberry varieties and five bulk soil samples, were sequenced with a high-throughput sequencing strategy. Based on these sequencing datasets, we profiled the taxonomical, functional, and phenotypic compositions of rhizosphere microbial communities for three different blueberry varieties and compared our results with a previous study focused on the rhizosphere microbiome of blueberry varieties. Our results demonstrated significant differences in alpha diversity and beta diversity of rhizosphere microbial communities of different blueberry varieties and bulk soil. The distribution patterns of taxonomical, functional, and phenotypic compositions of rhizosphere microbiome differ across the blueberry varieties. The rhizosphere microbial communities of three different blueberry varieties could be distinctly separated, and 28 discriminative biomarkers were selected to distinguish these three blueberry varieties. Core rhizosphere microbiota for blueberry was identified, and it contained 201 OTUs, which were mainly affiliated with Proteobacteria, Actinobacteria, and Acidobacteria. Moreover, the interactions between OTUs of blueberry rhizosphere microbial communities were explored by a co-occurrence network of OTUs from an ecological perspective.ConclusionsThis pilot study explored the characteristics of blueberry's rhizosphere microbial community, such as the beneficial microorganisms and core microbiome, and provided an integrative perspective on blueberry's rhizosphere microbiome, which beneficial to blueberry health and production.

Dataset Information

Competition for iron drives phytopathogen control by natural rhizosphere microbiomes.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets