Microorganisms have a pivotal role in the functioning of ecosystems. Recent studies have shown that microbial communities harbour keystone taxa, which drive community composition and function irrespective of their abundance. In this Opinion article, we propose a definition of keystone taxa in microbial ecology and summarize over 200 microbial keystone taxa that have been identified in soil, plant and marine ecosystems, as well as in the human microbiome. We explore the importance of keystone taxa and keystone guilds for microbiome structure and functioning and discuss the factors that determine their distribution and activities.

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Keystone taxa as drivers of microbiome structure and functioning

https://www.zora.uzh.ch/id/eprint/148899/1/Sasse_TIPS_2017.pdf

Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions. In this Review, Trivedi and colleagues explore the interactions between plants, their associated microbial communities and the environment, and also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.

Plant–microbiome interactions: from community assembly to plant health

Microbes of the phytomicrobiome are associated with every plant tissue and, in combination with the plant form the holobiont. Plants regulate the composition and activity of their associated bacterial community carefully. These microbes provide a wide range of services and benefits to the plant; in return, the plant provides the microbial community with reduced carbon and other metabolites. Soils are generally a moist environment, rich in reduced carbon which supports extensive soil microbial communities. The rhizomicrobiome is of great importance to agriculture owing to the rich diversity of root exudates and plant cell debris that attract diverse and unique patterns of microbial colonization. Microbes of the rhizomicrobiome play key roles in nutrient acquisition and assimilation, improved soil texture, secreting, and modulating extracellular molecules such as hormones, secondary metabolites, antibiotics, and various signal compounds, all leading to enhancement of plant growth. The microbes and compounds they secrete constitute valuable biostimulants and play pivotal roles in modulating plant stress responses. Research has demonstrated that inoculating plants with plant-growth promoting rhizobacteria (PGPR) or treating plants with microbe-to-plant signal compounds can be an effective strategy to stimulate crop growth. Furthermore, these strategies can improve crop tolerance for the abiotic stresses (e.g., drought, heat, and salinity) likely to become more frequent as climate change conditions continue to develop. This discovery has resulted in multifunctional PGPR-based formulations for commercial agriculture, to minimize the use of synthetic fertilizers and agrochemicals. This review is an update about the role of PGPR in agriculture, from their collection to commercialization as low-cost commercial agricultural inputs. First, we introduce the concept and role of the phytomicrobiome and the agricultural context underlying food security in the 21st century. Next, mechanisms of plant growth promotion by PGPR are discussed, including signal exchange between plant roots and PGPR and how these relationships modulate plant abiotic stress responses via induced systemic resistance. On the application side, strategies are discussed to improve rhizosphere colonization by PGPR inoculants. The final sections of the paper describe the applications of PGPR in 21st century agriculture and the roadmap to commercialization of a PGPR-based technology.

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Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture.

Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a “holobiont.” Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments. Reductionist approaches conducted under laboratory conditions have been critical to decipher the strategies used by specific microbes to cooperate and compete within or outside plant tissues. Nonetheless, our understanding of these microbial interactions in shaping more complex plant-associated microbial communities, along with their relevance for host health in a more natural context, remains sparse. Using examples obtained from reductionist and community-level approaches, we discuss the fundamental role of microbe-microbe interactions (prokaryotes and micro-eukaryotes) for microbial community structure and plant health. We provide a conceptual framework illustrating that interactions among microbiota members are critical for the establishment and the maintenance of host-microbial homeostasis.

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Microbial interactions within the plant holobiont.

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.

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

Genomic dissection of host–microbe and microbe–microbe interactions for advanced plant breeding

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 among 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.

/pdf/a-fungal-member-of-the-arabidopsis-thaliana-phyllosphere-1fptx2vz6x.pdf

A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme.


 Background: Leaves are primarily responsible for the plant's photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study we analyzed the temporal dynamics in the leaf microbiota of Arabidopsis thaliana, integrating changes in both, composition and microbe-microbe interactions via the study of microbial networks.Results: Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 'core' taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network 'hubs' and 'hubs' alternate with time. Conclusions: Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the possibility of predicting those patterns to drive microbial communities towards desired states.

/pdf/the-leaf-microbiota-of-arabidopsis-displays-reproducible-1a4bobr15j.pdf

The Leaf Microbiota of Arabidopsis Displays Reproducible Dynamics And Patterns Throughout The Growing Season

In natural habitats, plants are not only challenged by pathogenic organisms, but also extensively colonized by commensal microbes. The network of interactions that these microbes establish with their host and amongst each other has been suggested to contribute to the immune responses of plants against pathogens. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii has been shown to play an influential role in structuring the microbial communities of the leaf surface, known as phyllosphere. In this study, we show that the epiphytic yeast Moesziomyces albugensis, a close relative of pathogenic smut fungi, plays an antagonistic role in the microbial phyllosphere of Arabidopsis thaliana. In particular, M. albugensis prevents infection of A. thaliana by A. laibachii. Through a combination of transcriptome analysis and reverse genetics we identified a gene encoding a putative GH25 hydrolase as the major effector of the microbial antagonism of M. albugensis. 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 the development of novel biocontrol strategies.

/pdf/a-fungal-member-of-the-microbial-phyllosphere-antagonizes-4c59lhqgbd.pdf

A fungal member of the microbial phyllosphere antagonizes infection of Arabidopsis thaliana by the oomycete pathogen Albugo laibachii via a putative secreted hydrolase

Samuel Kroll

Papers

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

Genomic dissection of host–microbe and microbe–microbe interactions for advanced plant breeding

A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme.

The Leaf Microbiota of Arabidopsis Displays Reproducible Dynamics And Patterns Throughout The Growing Season

A fungal member of the microbial phyllosphere antagonizes infection of Arabidopsis thaliana by the oomycete pathogen Albugo laibachii via a putative secreted hydrolase