Abstract
Plant-associated microorganisms have been shown to critically affect host physiology and performance, suggesting that evolution and ecology of plants and animals can only be understood in a holobiont (host and its associated organisms) context. Host-associated microbial community structures are affected by abiotic and host factors, and increased attention is given to the role of the microbiome in interactions such as pathogen inhibition. However, little is known about how these factors act on the microbial community, and especially what role microbe–microbe interaction dynamics play. We have begun to address this knowledge gap for phyllosphere microbiomes of plants by simultaneously studying three major groups of Arabidopsis thaliana symbionts (bacteria, fungi and oomycetes) using a systems biology approach. We evaluated multiple potential factors of microbial community control: we sampled various wild A. thaliana populations at different times, performed field plantings with different host genotypes, and implemented successive host colonization experiments under lab conditions where abiotic factors, host genotype, and pathogen colonization was manipulated. Our results indicate that both abiotic factors and host genotype interact to affect plant colonization by all three groups of microbes. Considering microbe–microbe interactions, however, uncovered a network of interkingdom interactions with significant contributions to community structure. As in other scale-free networks, a small number of taxa, which we call microbial “hubs,” are strongly interconnected and have a severe effect on communities. By documenting these microbe–microbe interactions, we uncover an important mechanism explaining how abiotic factors and host genotypic signatures control microbial communities. In short, they act directly on “hub” microbes, which, via microbe–microbe interactions, transmit the effects to the microbial community. We analyzed two “hub” microbes (the obligate biotrophic oomycete pathogen Albugo and the basidiomycete yeast fungus Dioszegia) more closely. Albugo had strong effects on epiphytic and endophytic bacterial colonization. Specifically, alpha diversity decreased and beta diversity stabilized in the presence of Albugo infection, whereas they otherwise varied between plants. Dioszegia, on the other hand, provided evidence for direct hub interaction with phyllosphere bacteria. The identification of microbial “hubs” and their importance in phyllosphere microbiome structuring has crucial implications for plant–pathogen and microbe–microbe research and opens new entry points for ecosystem management and future targeted biocontrol. The revelation that effects can cascade through communities via “hub” microbes is important to understand community structure perturbations in parallel fields including human microbiomes and bioprocesses. In particular, parallels to human microbiome “keystone” pathogens and microbes open new avenues of interdisciplinary research that promise to better our understanding of functions of host-associated microbiomes.
Highlights
Hosts and their associated microbial communities are increasingly seen as inseparable entities whose ecology and evolution are inseparably entwined [1,2]
We show that interactions between microorganisms on plants can be responsible for large portions of observed microbial community structures on leaves
We discovered fungal and oomycete hub microbes that act by suppressing the growth and diversity of other microbes—even across kingdoms—and several candidate bacterial hubs, which largely positively control the abundance of other bacteria
Summary
Hosts and their associated microbial communities are increasingly seen as inseparable entities (metaorganisms) whose ecology and evolution are inseparably entwined [1,2]. Given the broad range of microbes that colonize above-ground parts of plants such as bacteria, yeasts, filamentous fungi [10], and protists [11], there is poor understanding of the entire diversity of those plant-associated microbes as well as factors that shape complex plant microbial communities from host colonization to plant senescence. How defined microbial communities get selected by different plant organs from highly variable and complex inoculum communities [14,15] is under strong debate. Since plant phenotypes and fitness depend on the associated microbiome, such knowledge is critical to enable plant microbiome management, that is, reaching the full potential of using microbes and microbial communities to promote beneficial plant–microbe interactions [2,16]
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