Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation.
Matthew T. Agler,Jonas Ruhe,Samuel Kroll,Constanze Morhenn,Sangtae Kim,Detlef Weigel,Eric Kemen +6 more
TLDR
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.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.read more
Citations
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Keystone taxa as drivers of microbiome structure and functioning
TL;DR: A definition of keystone taxa in microbial ecology is proposed and over 200 microbial keystoneTaxa that have been identified in soil, plant and marine ecosystems, as well as in the human microbiome are summarized.
Journal ArticleDOI
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
TL;DR: In this paper, physiological factors of plants that may govern plant-microbe interactions, focusing on root physiology and the role of root exudates, are discussed, and a possible sequence of events governing rhizobiome assembly is elaborated.
Journal ArticleDOI
Plant–microbiome interactions: from community assembly to plant health
TL;DR: This Review explores 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 and how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.
Journal ArticleDOI
Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture.
Rachel Backer,J. Stefan Rokem,Gayathri Ilangumaran,John R. Lamont,Dana Praslickova,Emily Ricci,Sowmyalakshmi Subramanian,Donald L. Smith +7 more
TL;DR: The concept and role of the phytomicrobiome and the agricultural context underlying food security in the 21st century are introduced and 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.
Journal ArticleDOI
Microbial interactions within the plant holobiont.
TL;DR: The fundamental role of microbe-microbe interactions (prokaryotes and micro-eukaryotes) for microbial community structure and plant health is discussed and a conceptual framework illustrating that interactions among microbiota members are critical for the establishment and the maintenance of host-microbial homeostasis is provided.
References
More filters
Journal ArticleDOI
The plant immune system
TL;DR: A detailed understanding of plant immune function will underpin crop improvement for food, fibre and biofuels production and provide extraordinary insights into molecular recognition, cell biology and evolution across biological kingdoms.
Journal ArticleDOI
Complex networks: Structure and dynamics
TL;DR: The major concepts and results recently achieved in the study of the structure and dynamics of complex networks are reviewed, and the relevant applications of these ideas in many different disciplines are summarized, ranging from nonlinear science to biology, from statistical mechanics to medicine and engineering.
Journal ArticleDOI
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
J. Gregory Caporaso,Christian L. Lauber,William A. Walters,Donna Berg-Lyons,James Huntley,Noah Fierer,Noah Fierer,Sarah M. Owens,Jason Betley,Louise Fraser,Markus J. Bauer,Niall Anthony Gormley,Jack A. Gilbert,Jack A. Gilbert,Geoff Smith,Rob Knight +15 more
TL;DR: It is shown that the protocol developed for these instruments successfully recaptures known biological results, and additionally that biological conclusions are consistent across sequencing platforms (the HiSeq2000 versus the MiSeq) and across the sequenced regions of amplicons.
Journal ArticleDOI
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity
Marcel G. A. van der Heijden,John N. Klironomos,Margot Ursic,Peter Moutoglis,R. Streitwolf-Engel,Thomas Boller,Andres Wiemken,Ian R. Sanders +7 more
TL;DR: It is shown that below-ground diversity of arbuscular mycorrhizal fungi (AMF) is a major factor contributing to the maintenance of plant biodiversity and to ecosystem functioning, and that microbial interactions can drive ecosystem functions such as plant biodiversity, productivity and variability.
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