Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation.
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.
Project description:Recent research suggested that plants behave differently under combined versus single abiotic and biotic stress conditions in controlled environments. While this work has provided a glimpse into how plants might behave under complex natural conditions, it also highlights the need for field experiments using established model systems. In nature, diverse microbes colonize the phyllosphere of Arabidopsis thaliana, including the obligate biotroph oomycete genus Albugo, causal agent of the common disease white rust. Biotrophic, as well as hemibiotrophic plant pathogens are characterized by efficient suppression of host defense responses. Lab experiments have even shown that Albugo sp. can suppress non-host resistance, thereby enabling otherwise avirulent pathogen growth. We asked how a pathogen that is vitally dependent on a living host can compete in nature for limited niche space while paradoxically enabling colonization of its host plant for competitors? To address this question, we used a proteomics approach to identify differences and similarities between lab and field samples of Albugo sp.-infected and -uninfected A. thaliana plants. We could identify highly similar apoplastic proteomic profiles in both infected and uninfected plants. In wild plants, however, a broad range of defense-related proteins were detected in the apoplast regardless of infection status, while no or low levels of defense-related proteins were detected in lab samples. These results indicate that Albugo sp. do not strongly affect immune responses and leave distinct branches of the immune signaling network intact. To validate our findings and to get mechanistic insights, we tested a panel of A. thaliana mutant plants with induced or compromised immunity for susceptibility to different biotrophic pathogens. Our findings suggest that the biotroph pathogen Albugo selectively interferes with host defense under different environmental and competitive pressures to maintain its ecological niche dominance. Adaptation to host immune responses while maintaining a partially active host immunity seems advantageous against competitors. We suggest a model for future research that considers not only host-microbe but in addition microbe-microbe and microbe-host environment factors.
Project description:The phyllosphere referred to the total aerial plant surfaces (above-ground portions), as habitat for microorganisms. Microorganisms establish compositionally complex communities on the leaf surface. The microbiome of phyllosphere is rich in diversity of bacteria, fungi, actinomycetes, cyanobacteria, and viruses. The diversity, dispersal, and community development on the leaf surface are based on the physiochemistry, environment, and also the immunity of the host plant. A colonization process is an important event where both the microbe and the host plant have been benefited. Microbes commonly established either epiphytic or endophytic mode of life cycle on phyllosphere environment, which helps the host plant and functional communication with the surrounding environment. To the scientific advancement, several molecular techniques like metagenomics and metaproteomics have been used to study and understand the physiology and functional relationship of microbes to the host and its environment. Based on the available information, this chapter describes the basic understanding of microbiome in leaf structure and physiology, microbial interactions, especially bacteria, fungi, and actinomycetes, and their adaptation in the phyllosphere environment. Further, the detailed information related to the importance of the microbiome in phyllosphere to the host plant and their environment has been analyzed. Besides, biopotentials of the phyllosphere microbiome have been reviewed.
Project description:BACKGROUND:The phyllosphere is an important microbial habitat, but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited. In this study, we quantify bacterial functional diversity in the phyllosphere of 17 tree species in a diverse neotropical forest using metagenomic shotgun sequencing. We ask how hosts drive the functional composition of phyllosphere communities and their turnover across tree species, using host functional traits and phylogeny. RESULTS:Neotropical tree phyllosphere communities are dominated by functions related to the metabolism of carbohydrates, amino acids, and energy acquisition, along with environmental signalling pathways involved in membrane transport. While most functional variation was observed within communities, there is non-random assembly of microbial functions across host species possessing different leaf traits. Metabolic functions related to biosynthesis and degradation of secondary compounds, along with signal transduction and cell-cell adhesion, were particularly important in driving the match between microbial functions and host traits. These microbial functions were also evolutionarily conserved across the host phylogeny. CONCLUSIONS:Functional profiling based on metagenomic shotgun sequencing offers evidence for the presence of a core functional microbiota across phyllosphere communities of neotropical trees. While functional turnover across phyllosphere communities is relatively small, the association between microbial functions and leaf trait gradients among host species supports a significant role for plant hosts as selective filters on phyllosphere community assembly. This interpretation is supported by the presence of phylogenetic signal for the microbial traits driving inter-community variation across the host phylogeny. Taken together, our results suggest that there is adaptive matching between phyllosphere microbes and their plant hosts. Video abstract.
Project description:Microbes constitute a vital part of the plant holobiont. They establish plant-microbe or microbe-microbe associations, forming a unique microbiota with each plant species and under different environmental conditions. These microbial communities have to adapt to diverse environmental conditions, such as geographical location, climate conditions and soil types, and are subjected to changes in their surrounding environment. Elevated ozone concentration is one of the most important aspects of global change, but its effect on microbial communities living on plant surfaces has barely been investigated. In the current study, we aimed at elucidating the potential effect of elevated ozone concentrations on the phyllosphere (aerial part of the plant) and rhizoplane (surface of the root) microbiota by adopting next-generation 16S rRNA amplicon sequencing. A standard japonica rice cultivar Nipponbare and an ozone-tolerant breeding line L81 (Nipponbare background) were pre-grown in a greenhouse for 10 weeks and then exposed to ozone at 85 ppb for 7 h daily for 30 days in open top chambers. Microbial cells were collected from the phyllosphere and rhizoplane separately. The treatment or different genotypes did not affect various diversity indices. On the other hand, the relative abundance of some bacterial taxa were significantly affected in the rhizoplane community of ozone-treated plants. A significant effect of ozone was detected by homogeneity of molecular variance analysis in the phyllosphere, meaning that the community from ozone-treated phyllosphere samples was more variable than those from control plants. In addition, a weak treatment effect was observed by clustering samples based on the Yue and Clayton and weighted UniFrac distance matrices among samples. We therefore conclude that the elevated ozone concentrations affected the bacterial community structure of the phyllosphere and the rhizosplane as a whole, even though this effect was rather weak and did not lead to changes of the function of the communities.
Project description:We report the draft genome sequences of type strains for Dioszegia crocea and its closely related species Dioszegia aurantiaca, which should improve our understanding of the epiphytic phylloplane yeasts. These data will also have implications for the plant microbiome, since Dioszegia is considered a microbial "hub" taxon.
Project description:Plants are now recognized as metaorganisms which are composed of a host plant associated with a multitude of microbes that provide the host plant with a variety of essential functions to adapt to the local environment. Recent research showed the remarkable importance and range of microbial partners for enhancing the growth and health of plants. However, plant-microbe holobionts are influenced by many different factors, generating complex interactive systems. In this review, we summarize insights from this emerging field, highlighting the factors that contribute to the recruitment, selection, enrichment, and dynamic interactions of plant-associated microbiota. We then propose a roadmap for synthetic community application with the aim of establishing sustainable agricultural systems that use microbial communities to enhance the productivity and health of plants independently of chemical fertilizers and pesticides. Considering global warming and climate change, we suggest that desert plants can serve as a suitable pool of potentially beneficial microbes to maintain plant growth under abiotic stress conditions. Finally, we propose a framework for advancing the application of microbial inoculants in agriculture.
Project description:Morphological and chemical differences between plant genera influence phyllosphere microbial populations, but the factors driving within-species variation in phyllosphere populations are poorly understood. Twenty-six lettuce accessions were used to investigate factors controlling within-species variation in phyllosphere bacterial populations. Morphological and physiochemical characteristics of the plants were compared, and bacterial community structure and diversity were investigated using terminal restriction fragment length polymorphism (T-RFLP) profiling and 16S rRNA gene clone libraries. Plant morphology and levels of soluble carbohydrates, calcium, and phenolic compounds (which have long been associated with plant responses to biotic stress) were found to significantly influence bacterial community structure. Clone libraries from three representative accessions were found to be significantly different in terms of both sequence differences and the bacterial genera represented. All three libraries were dominated by Pseudomonas species and the Enterobacteriaceae family. Significant differences in the relative proportions of genera in the Enterobacteriaceae were detected between lettuce accessions. Two such genera (Erwinia and Enterobacter) showed significant variation between the accessions and revealed microbe-microbe interactions. We conclude that both leaf surface properties and microbial interactions are important in determining the structure and diversity of the phyllosphere bacterial community.
Project description:The phyllosphere microbiome is increasingly recognised as an influential component of plant physiology, yet it remains unclear whether stable host-microbe associations generally exist in the phyllosphere. Leptospermum scoparium (m?nuka) is a tea tree indigenous to New Zealand, and honey derived from m?nuka is widely known to possess unique antimicrobial properties. However, the host physiological traits associated with these antimicrobial properties vary widely, and the specific cause of such variation has eluded scientists despite decades of research. Notably, the m?nuka phyllosphere microbiome remains uncharacterised, and its potential role in mediating host physiology has not been considered. Working within the prevailing core microbiome conceptual framework, we hypothesise that the phyllosphere microbiome of m?nuka exhibits specific host association patterns congruent with those of a microbial community under host selective pressure (null hypothesis: the m?nuka phyllosphere microbiome is recruited stochastically from the surrounding environment). To examine our hypothesis, we characterised the phyllosphere and associated soil microbiomes of five distinct and geographically distant m?nuka populations across the North Island of New Zealand. We identified a habitat-specific and relatively abundant core microbiome in the m?nuka phyllosphere, which was persistent across all samples. In contrast, non-core phyllosphere microorganisms exhibited significant variation across individual host trees and populations that was strongly driven by environmental and spatial factors. Our results demonstrate the existence of a dominant and ubiquitous core microbiome in the phyllosphere of m?nuka, supporting our hypothesis that phyllosphere microorganisms of m?nuka exhibit specific host association and potentially mediate physiological traits of this nationally and culturally treasured indigenous plant. In addition, our results illustrate biogeographical patterns in m?nuka phyllosphere microbiomes and offer insight into factors contributing to phyllosphere microbiome assembly.
Project description:The phyllosphere supports a tremendous diversity of microbes, which have the potential to influence plant biogeography and ecosystem function. Although biocontrol agents (BCAs) have been used extensively for controlling plant diseases, the ecological effects of BCAs on phyllosphere bacteria and the relationships between phyllosphere community and plant health are poorly understood. In this study, we explored the control efficiency of two BCA communities on bacterial wildfire disease by repeatedly spraying BCAs on tobacco leaves. The results of field tests showed that BCAs used in our study, especially BCA_B, had remarkable control effects against tobacco wildfire disease. The higher control efficiency of BCA_B might be attributed to a highly diverse and complex community in the phyllosphere. By 16S ribosomal RNA gene sequencing, we found that phyllosphere microbial community, including community diversity, taxonomic composition and microbial interactions, changed significantly by application of BCAs. According to the correlation analysis, it showed that wildfire disease infection of plants was negatively related to phyllosphere microbial diversity, indicating a highly diverse community in the phyllosphere might prevent pathogens invasion and colonization. In addition, we inferred that a more complex network in the phyllosphere might be beneficial for decreasing the chances of bacterial wildfire outbreak, and the genera of Pantoea and Sphingomonas might play important roles in wildfire disease suppression. These correlations between phyllosphere community and plant health will improve our understanding on the ecological function of phyllosphere community on plants.
Project description:Background: The phyllosphere hosts a variety of microorganisms, including bacteria, which can play a positive role in the success of the host plant. Bacterial communities in the phylloplane are influenced by both biotic and abiotic factors, including host plant surface topography and chemistry, which change in concert with microbial communities as the plant leaves develop and age. Methods: We examined how the Zea mays L. leaf microbial community structure changed with plant age. Ribosomal spacer length and scanning electron microscopic imaging strategies were used to assess microbial community composition across maize plant ages, using a novel staggered experimental design. Results: Significant changes in community composition were observed for both molecular and imaging analyses, and the two analysis methods provided complementary information about bacterial community structure within each leaf developmental stage. Conclusions: Both taxonomic and cell-size trait patterns provided evidence for niche-based contributions to microbial community development on leaves.