Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation

By Matthew T. Agler, Jonas Ruhe, Samuel Kroll, Constanze Morhenn, Sang-Tae Kim, Detlef Weigel, E. Kemen. PLoS Biology, 2016

1,187 citations recorded by the source corpus.

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.

Subfields: Cell Biology, Plant Science

View Paper: https://www.semanticscholar.org/paper/cffee72c5f0aa9590bc0c03ffc0c52c93e829c88

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Citations in the corpus

Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming (2018, background): “significantly influence community composition [37].”
Microbial interactions within the plant holobiont (2018, positive): “Although these correlations do not necessarily predict causal relationships [210], analysis of plant-associated microbial networks tends to indicate that positive correlations dominate among microbes from the same kingdom, whereas negative interactions primarily occur through inter-kingdom microbemi”
Prospecting the characteristics and significance of the phyllosphere microbiome (2018, background): “…content, leaf age, ultraviolet light, relative humidity, soil and biotic factors such as pathogens, nematodes, or insects, and most importantly, the host genotype and other plants present in the surroundings (BalintKurti et al. 2010; Hunter et al. 2010; Humphrey et al. 2014; Agler et al. 2016).”
Forest Tree Microbiomes and Associated Fungal Endophytes: Functional Roles and Impact on Forest Health (2019, background): “Interestingly, the control of plant microbiomes by abiotic factors and host genotype features could be achieved via a small number of microbial taxa, so-called microbial “hubs”, as was recently demonstrated [30].”
Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots (2018, background): “It has also been observed that the impact of abiotic factors and host genotypes on the 70 plant microbiome is facilitated via keystone taxa [46], and the root microbial network 71 complexity is linked to plant survival [47].”
Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival (2018, positive): “We characterized the multi-kingdommicrobial consortia along the soil-root continuum by simultaneous DNA amplicon sequencing of the bacterial 16S rRNA gene and fungal, as well as oomycetal, internal transcribed spacer (ITS) regions (Agler et al., 2016) (Table S2).”
NetCoMi: network construction and comparison for microbiome data in R (2020, neutral): “A set of most central nodes can be defined in two ways: In the first approach, under the assumption that the centrality values are log-normal distributed [84], the set of most central nodes contains nodes with a centrality value greater than a certain quantile of the fitted log-normal distribution.”