Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen

Abstract

The aerial parts of plants are host to taxonomically structured bacterial communities. Members of the core phyllosphere microbiota can protect Arabidopsis thaliana against foliar pathogens. However, whether plant protection is widespread and to what extent the modes of protection differ among phyllosphere microorganisms is not clear. Here, we present a systematic analysis of plant protection capabilities of the At -LSPHERE, which is a collection of >200 bacterial isolates from Arabidopsis thaliana, against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. In total 224 bacterial leaf isolates were individually assessed for plant protection in a gnotobiotic system. Protection against the pathogen varied with approximately 10% of leaf microbiota strains providing full protection, 10% showing intermediate levels of protection and the remaining 80% not markedly reducing disease phenotypes upon infection. The most protective strains were distributed across different taxonomic groups. Synthetic community experiments revealed additive effects of strains but also that a single strain can confer full protection in a community context. We also identify different mechanisms that contribute to plant protection. Although pattern-triggered immunity co-receptor signaling is involved in protection by a subset of strains, other strains protected in the absence of functional plant immunity receptors BAK1 and BKK1. Using a comparative genomics approach combined with mutagenesis, we reveal that direct bacteria-pathogen interactions contribute to plant protection by Rhizobium Leaf202. This shows that a computational approach based on the data provided can be used to identify genes of the microbiota that are important for plant protection.

Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ

“…To study the interaction between phyllosphere microbiota strains, we selected two representative strains from the Alphaproteobacteria, the most abundant bacterial class found on A. thaliana leaves 26 . Among Alphaproteobacteria the bacterial families of Sphingomonadaceae and Rhizobiaceaea are the most common and include strains with plant beneficial functions 20 , 21 , 29 , 50 , 53 . Previous experiments have shown that the genera of Sphingomonas and Rhizobium have the potential to affect community assembly and structure 27 .…”

Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom

“… 2021 , Vogel et al . 2021 ). Based on these findings one could thus speculate that the continued coevolution of fungal broad host-range pathogens with plant holobionts predominantly favors the evolution of effectors that, despite narrow activity spectra, function in nearly any holobiont.…”

Commensal Pseudomonas fluorescens Strains Protect Arabidopsis from Closely Related Pseudomonas Pathogens in a Colonization-Dependent Manner

“…This suggests that N2C3 is an opportunistic pathogen and the presence of beneficial microbes in the rhizosphere may lead to protection against N2C3 pathogenesis. While other models exist to study microbial protection against plant pathogens, they have largely focused on leaf pathogens ( 18 , 19 ); thus our system involving N2C3 and Pseudomonas strains provides a unique opportunity to understand how members of the rhizosphere microbiome can protect against pathogens.…”