Plants are not only challenged by pathogenic organisms, but also colonized by commensal microbes. The network of interactions these microbes establish with their host and amongst each other is suggested to contribute to the immune responses of plants against pathogens. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii plays an influential role in structuring the leaf phyllosphere. We show that the epiphytic yeast Moesziomyces bullatus ex Albugo on Arabidopsis, a close relative of pathogenic smut fungi, is an antagonistic member of the A. thaliana phyllosphere, which reduces infection of A. thaliana by A. laibachii. Combination of transcriptomics, reverse genetics and protein characterization identified a GH25 hydrolase with lysozyme activity as a major effector of this microbial antagonism. Our findings broaden the understanding of microbial interactions within the phyllosphere, provide insights into the evolution of epiphytic basidiomycete yeasts and pave the way for novel biocontrol strategies.
In natural habitats, plants are challenged by pathogenic organisms, while they are extensively colonized by microbes, which establish a network of interactions with the plant and amongst each other. Therefore, plant immunity might not only be shaped by the co-evolutionary arms race between plants and pathogens, but also be a result from interactions within the microbiota and the host. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii has been identified as main driver of the phyllosphere microbiota. In this study, we describe the epiphytic yeast Moesziomyces albugensis and its antagonistic role in the microbial phyllosphere of Arabidopsis thaliana. M. albugensis, a close relative to pathogenic smut fungi, antagonizes several leaf-colonizing microbes. In particular, it prevents infection of A. thaliana by A. laibachii. Combination of transcriptomics and reverse genetics identified a gene of M. albugensis encoding a GH25 hydrolase as major factor of this microbial antagonism. Findings in this study provide identify a potential factor of oomycete biocontrol, provide mechanistic insight in microbial antagonism shaping leaf microbiota and provide new insights in the evolution of epiphytic basidiomycete yeasts. Recent research has focused largely on the importance of rhizoshpere microbiota in nutrient acquisition, pathogenic protection, and boosting overall plant growth and development [1-3]. However, the above ground parts of the plant including the phyllosphere are colonized by diverse groups of microbes that assist in plant protection and immunity [4,5] . The environment has a greater impact on the microbial community on the leaf surface, ultimately influencing the host-microbe interactions [6]. Scale-free network analysis was performed with the leaf microbial population of Arabidopsis thaliana [7]. Majority of the interactions existing in the network were found to be negative, consistent with the fact that it is rather the antagonistic interactions that stabilizes a microbial community [8]. Phyllosphere network analysis 3 of A. thaliana revealed a small number of microbes as hub organisms that have severe effect on the community structure. The major hub microbe in the A. thaliana phyllosphere is the oomycete Albugo laibachii, which is a biotrophic pathogen of Arabidopsis. This pathogen has been shown to significantly reduce the bacterial diversity of epiphytic and endophytic leaf habitats. Since bacteria generally comprises a large proportion of the phyllosphere microbiome, [9]; phylogenetic profiling of A. thaliana was also directed towards identifying a small group of bacteria that frequently colonize A. thaliana leaves. The analysis helped to develop a synthetic community of bacteria for gnotobiotic experiments. Along with bacteria and oomycetes, a broad range of fungi are colonizers of the A. thaliana leaf. Among those fungi, basidiomycete yeasts are frequently found and the most frequent ones is the epiphytic basidiomycete genus Dioszegia, as well as an anamorphic yeast classifie...
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