A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees

Shakya, Migun; Gottel, Neil; Castro, Hector F.; Yang, Zamin K.; Gunter, Lee E.; Labbé, Jessy; Muchero, Wellington; Bonito, Gregory; Vilgalys, Rytas; Tuskan, Gerald A.; Podar, Mircea; Schadt, Christopher W.

doi:10.1371/journal.pone.0076382

Cited by 252 publications

(256 citation statements)

References 61 publications

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“…Likewise, there was an increased abundance of Anaerolineae (Chloroflexi), Clostridia (Firmicutes), and a subpopulation of Actinobacteria (Saccharothrix spp., unclassified Actinosynnemataceae) in R plants under paddy and upland conditions. In another study, Shakya et al (2013) showed that a high percentage (more than 90%) of operational taxonomic units (OTUs) specific to sampled mature Populus deltoides trees from two watersheds of North Carolina and Tennessee in two seasons (spring and fall) had the dominant phyla Proteobacteria (56.1%), Actinobacteria (17.5%), and Acidobacteria (10%). However, dominance of Proteobacteria was replaced by Actinobacteria from spring to fall in the Tennessee samples.…”

Section: Determination Of Microbiome By Host Host Genotypementioning

confidence: 99%

“…This study did not directly explain any host-specific variance in rhizospheric bacterial community structure, instead postulating an indirect influence of changing soil properties (through rhizodeposits and exudates) that showed statistically significant influence on the rhizospheric microbiome. These studies (Ikeda et al, 2011;Shakya et al, 2013) still pose open-ended questions. What are the specific genes/alleles that control microbial communities?…”

Section: Determination Of Microbiome By Host Host Genotypementioning

confidence: 99%

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Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem

2014

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There is considerable evidence in the literature that beneficial rhizospheric microbes can alter plant morphology, enhance plant growth, and increase mineral content. Of late, there is a surge to understand the impact of the microbiome on plant health. Recent research shows the utilization of novel sequencing techniques to identify the microbiome in model systems such as Arabidopsis (Arabidopsis thaliana) and maize (Zea mays). However, it is not known how the community of microbes identified may play a role to improve plant health and fitness. There are very few detailed studies with isolated beneficial microbes showing the importance of the functional microbiome in plant fitness and disease protection. Some recent work on the cultivated microbiome in rice (Oryza sativa) shows that a wide diversity of bacterial species is associated with the roots of field-grown rice plants. However, the biological significance and potential effects of the microbiome on the host plants are completely unknown. Work performed with isolated strains showed various genetic pathways that are involved in the recognition of host-specific factors that play roles in beneficial host-microbe interactions. The composition of the microbiome in plants is dynamic and controlled by multiple factors. In the case of the rhizosphere, temperature, pH, and the presence of chemical signals from bacteria, plants, and nematodes all shape the environment and influence which organisms will flourish. This provides a basis for plants and their microbiomes to selectively associate with one another. This Update addresses the importance of the functional microbiome to identify phenotypes that may provide a sustainable and effective strategy to increase crop yield and food security.

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Section: Determination Of Microbiome By Host Host Genotypementioning

confidence: 99%

Section: Determination Of Microbiome By Host Host Genotypementioning

confidence: 99%

Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem

2014

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“…Recent studies have used high-throughput sequencing to provide new insights into the bacterial composition and organization of different plant microbiomes, including Arabidopsis, Populus, and maize (9)(10)(11)(12)(13)(14). Detailed characterization of the core root microbiome of Arabidopsis (9)(10)(11) showed that the dominant phyla inside the root (the endosphere) are much less diverse than the phyla in the soil around the root (the rhizosphere), and a potential core root microbiome could be identified.…”

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confidence: 99%

“…A recent study in maize examined microbiome variation across many different inbred lines at different sites and found a large variation arising from geographical location between three different states in the United States and a relatively smaller dependence on the genotype (12). Although the microbiomes examined in the maize study consisted of combined rhizospheric and endospheric microbes (12), a study in poplar found that the variation between locations in two different states affected both rhizospheric and endospheric microbes (14).…”

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confidence: 99%

Structure, variation, and assembly of the root-associated microbiomes of rice

Edwards¹,

Johnson²,

Santos‐Medellín³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

2,078

216

1,607

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Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.

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“…Actinomycetes and pseudomonads represent two of the major groups of bacteria found in soils and rhizospheres (16,17) and are likely to simultaneously utilize similar resources, such as iron, or even to compete for them. Both groups produce siderophores to take up this essential element, but different types of molecules are produced by the two groups.…”

mentioning

confidence: 99%

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

Galet

Deveau

Hôtel

et al. 2015

Appl Environ Microbiol

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Iron is essential in many biological processes. However, its bioavailability is reduced in aerobic environments, such as soil. To overcome this limitation, microorganisms have developed different strategies, such as iron chelation by siderophores. Some bacteria have even gained the ability to detect and utilize xenosiderophores, i.e., siderophores produced by other organisms. We illustrate an example of such an interaction between two soil bacteria, Pseudomonas fluorescens strain BBc6R8 and Streptomyces ambofaciens ATCC 23877, which produce the siderophores pyoverdine and enantiopyochelin and the siderophores desferrioxamines B and E and coelichelin, respectively. During pairwise cultures on iron-limiting agar medium, no induction of siderophore synthesis by P. fluorescens BBc6R8 was observed in the presence of S. ambofaciens ATCC 23877. Cocultures with a Streptomyces mutant strain that produced either coelichelin or desferrioxamines, as well as culture in a medium supplemented with desferrioxamine B, resulted in the absence of pyoverdine production; however, culture with a double mutant deficient in desferrioxamines and coelichelin production did not. This strongly suggests that P. fluorescens BBbc6R8 utilizes the ferrioxamines and ferricoelichelin produced by S. ambofaciens as xenosiderophores and therefore no longer activates the production of its own siderophores. A screening of a library of P. fluorescens BBc6R8 mutants highlighted the involvement of the TonB-dependent receptor FoxA in this process: the expression of foxA and genes involved in the regulation of its biosynthesis was induced in the presence of S. ambofaciens. In a competitive environment, such as soil, siderophore piracy could well be one of the driving forces that determine the outcome of microbial competition. Bacteria detect, assimilate, and integrate different environmental signals in order to better adapt to their habitat and cope with changes in environmental conditions. Multiple signaling pathways allow them to communicate with each other within the same species or between different species (1). This can be achieved through the production and detection of diffusible molecules in the environment. In response to these interactions, the microorganisms have developed complex metabolic and physiological responses. One of the essential environmental factors vital for organisms is iron. It plays an essential role in many biological processes, such as DNA synthesis, respiration, and photosynthesis. Iron can adopt two different ionic forms, Fe 2ϩ and Fe 3ϩ . This property makes it an important player in the oxidation-reduction reactions in the cell. However, while iron is an abundant element on earth, its bioavailability is reduced in aerobic environments, such as soil. Ferric iron (Fe 3ϩ ) forms insoluble ferric hydroxides (with a solubility product of ϳ10 Ϫ39 ) in the presence of oxygen (2-4). Therefore, iron is a limiting factor for the growth of microorganisms.To overcome the limitation of iron bioavailability, aerobic bacteria have develop...

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A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees

Cited by 252 publications

References 61 publications

Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem

Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem

Structure, variation, and assembly of the root-associated microbiomes of rice

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

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