Influence of Tall Fescue Epichloë endophytes on Rhizosphere Soil Microbiome

Abstract Background Tall fescue (Lolium arundinaceum (Schreb.) S.J. Darbyshire) is a popular perennial grass species for livestock production and amenities in the United States. Tall fescue often forms a symbiotic relationship with fungal endophytes (Epichloë coenophiala) which provides increased plant tolerance to environmental stress compared to endophyte-free plants. However, whether this improved plant performance is the sole result of the unique relationship between the grass and the shoot-dwelling fungal endophyte of rhizosphere origin remains a question. This symbiosis possibly regulates the recruitment of beneficial soil microbial communities in endophyte-infected tall fescue rhizosphere and may offer enhanced nutrients and water acquisition, thereby, providing the plant with an increased tolerance level against environmental stresses. We compared the soil bacterial and fungal community composition and investigated possible community shifts in soil microbial populations based on endophyte infection in tall fescue by analyzing the 16s rRNA gene and ITS specific region. Results Our data revealed that bacterial community richness and the evenness indicated by Shannon Diversity Index (SDI) was greater than 4 in both endophyte-infected and endophyte-free tall fescue soil. In both types tall fescue soil, the prominent bacterial families were Planctomycetaceae, Balstocatellaceae_(subgroup_4), Chitinophagaceae, and Bacillaceae. In the case of soil fungal diversity, the SDI was overall low and ranged between 1.21 for endophyte-free and 1.27 for endophyte-infected tall fescue soil. The prominent fungal phyla were Basidiomycota and Ascomycota, and we observed a clear fungal community difference between endophyte-infected and endophyte-free soil at the phylum level. Moreover, endophyte-infected tall fescue soil showed a greater diversity at the genus level compared to endophyte-free tall fescue soil. In addition, plant-available soil phosphorus (P) is also influenced by the presence of endophytes in tall fescue. Conclusion Our results indicate that there is a tripartite relationship between tall fescue, the presence of fungal endophyte in the tall fescue, and the below-ground soil fungal communities. The dynamic of this three-way interaction perhaps contributes to the nutrient acquisition and stress tolerance by tall fescue possibly by recruiting a diverse array of potentially beneficial soil microbes.

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Influence of Tall Fescue Epichloë Endophytes on Rhizosphere Soil Microbiome

Microorganisms ◽

10.3390/microorganisms9091843 ◽

2021 ◽

Vol 9 (9) ◽

pp. 1843

Author(s):

Kishan Mahmud ◽

Kendall Lee ◽

Nicholas S. Hill ◽

Anaas Mergoum ◽

Ali Missaoui

Keyword(s):

Tall Fescue ◽

Fungal Community ◽

Fungal Endophytes ◽

Plant Performance ◽

Soil Microbiome ◽

Available Phosphorus ◽

Rrna Gene ◽

Bacterial Phyla ◽

Endophyte Infection ◽

Soil Bacterial

Tall fescue (Lolium arundinaceum (Schreb.) S.J. Darbyshire) often forms a symbiotic relationship with fungal endophytes (Epichloë coenophiala), which provides increased plant performance and greater tolerance to environmental stress compared to endophyte-free tall fescue. Whether this enhanced performance of tall fescue exclusively results from the grass–fungus symbiosis, or this symbiosis additionally results in the recruitment of soil microbes in the rhizosphere that in turn promote plant growth, remain a question. We investigated the soil bacterial and fungal community composition in iron-rich soil in the southeastern USA, and possible community shifts in soil microbial populations based on endophyte infection in tall fescue by analyzing the 16s rRNA gene and ITS specific region. Our data revealed that plant-available phosphorus (P) was significantly (p < 0.05) influenced by endophyte infection in tall fescue. While the prominent soil bacterial phyla were similar, a clear fungal community shift was observed between endophyte-infected (E+) and endophyte-free (E−) tall fescue soil at the phylum level. Moreover, compared to E− soil, E+ soil showed a greater fungal diversity at the genus level. Our results, thus, indicate a possible three-way interaction between tall fescue, fungal endophyte, and soil fungal communities resulting in improved tall fescue performance.

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Infection with a Shoot-Specific Fungal Endophyte (Epichloë) Alters Tall Fescue Soil Microbial Communities

Microbial Ecology ◽

10.1007/s00248-016-0750-8 ◽

2016 ◽

Vol 72 (1) ◽

pp. 197-206 ◽

Cited By ~ 28

Author(s):

Xavier Rojas ◽

Jingqi Guo ◽

Jonathan W. Leff ◽

David H. McNear ◽

Noah Fierer ◽

...

Keyword(s):

Microbial Communities ◽

Tall Fescue ◽

Soil Microbial Communities ◽

Fungal Endophyte ◽

Soil Microbial

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Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations

mSystems ◽

10.1128/msystems.00061-19 ◽

2019 ◽

Vol 4 (4) ◽

Cited By ~ 9

Author(s):

Taniya Roy Chowdhury ◽

Joon-Yong Lee ◽

Eric M. Bottos ◽

Colin J. Brislawn ◽

Richard Allen White ◽

...

Keyword(s):

Climate Change ◽

United States ◽

Soil Moisture ◽

Metabolic Pathways ◽

Soil Microbial Communities ◽

The United States ◽

Soil Microbiome ◽

Soil Drying ◽

Soil Microbial ◽

And Function

ABSTRACT Climate change is causing shifts in precipitation patterns in the central grasslands of the United States, with largely unknown consequences on the collective physiological responses of the soil microbial community, i.e., the metaphenome. Here, we used an untargeted omics approach to determine the soil microbial community’s metaphenomic response to soil moisture and to define specific metabolic signatures of the response. Specifically, we aimed to develop the technical approaches and metabolic mapping framework necessary for future systematic ecological studies. We collected soil from three locations at the Konza Long-Term Ecological Research (LTER) field station in Kansas, and the soils were incubated for 15 days under dry or wet conditions and compared to field-moist controls. The microbiome response to wetting or drying was determined by 16S rRNA amplicon sequencing, metatranscriptomics, and metabolomics, and the resulting shifts in taxa, gene expression, and metabolites were assessed. Soil drying resulted in significant shifts in both the composition and function of the soil microbiome. In contrast, there were few changes following wetting. The combined metabolic and metatranscriptomic data were used to generate reaction networks to determine the metaphenomic response to soil moisture transitions. Site location was a strong determinant of the response of the soil microbiome to moisture perturbations. However, some specific metabolic pathways changed consistently across sites, including an increase in pathways and metabolites for production of sugars and other osmolytes as a response to drying. Using this approach, we demonstrate that despite the high complexity of the soil habitat, it is possible to generate insight into the effect of environmental change on the soil microbiome and its physiology and functions, thus laying the groundwork for future, targeted studies. IMPORTANCE Climate change is predicted to result in increased drought extent and intensity in the highly productive, former tallgrass prairie region of the continental United States. These soils store large reserves of carbon. The decrease in soil moisture due to drought has largely unknown consequences on soil carbon cycling and other key biogeochemical cycles carried out by soil microbiomes. In this study, we found that soil drying had a significant impact on the structure and function of soil microbial communities, including shifts in expression of specific metabolic pathways, such as those leading toward production of osmoprotectant compounds. This study demonstrates the application of an untargeted multi-omics approach to decipher details of the soil microbial community’s metaphenotypic response to environmental perturbations and should be applicable to studies of other complex microbial systems as well.

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Changes in Bacterial and Fungal Community of Soil under Treatment of Pesticides

Agronomy ◽

10.3390/agronomy12010124 ◽

2022 ◽

Vol 12 (1) ◽

pp. 124

Author(s):

Rostislav Streletskii ◽

Angelika Astaykina ◽

George Krasnov ◽

Victor Gorbatov

Keyword(s):

Fungal Community ◽

Large Scale ◽

High Throughput Sequencing ◽

Soil Microbial Communities ◽

Illumina Miseq ◽

Soil Microbiome ◽

Soil Microbial ◽

Large Scale Assessment ◽

Integral Methods ◽

State Registration

Experiments were carried out in soil microcosms with the treatment of pesticide formulations—imidacloprid, benomyl, and metribuzin in single and tenfold application rates. For additional stimulation of microorganisms, a starch–mineral mixture was added to some variants. For all samples, high-throughput sequencing on the Illumina MiSeq platform of the V4 (16S rRNA) and ITS1 (18S rRNA) fragments was carried out. As a result, it was possible to establish the characteristic changes in the structure of the soil fungal and bacterial communities under pesticides application. The application of pesticides was accompanied by dramatic shifts in alfa-diversity of the fungal community. The phylum Basidiomycota was likely to be involved in the degradation of pesticides. The changes in the relative abundance of the genera Terrabacter, Kitasatospora, Streptomyces, Sphingomonas, Apiotrichum, Solicoccozyma, Gamsia, and Humicola can be proposed as an indicator of pesticide contamination. It is suggested to use these markers for large-scale assessment of the effect of pesticides on soil microbial communities instead of classical integral methods, including within the framework of state registration of pesticides. It is also recommended to research the effect of pesticides on the soil microbiome during artificially initiated successions using the additional source of carbon.

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Do Bioinoculants Affect Resident Microbial Communities? A Meta-Analysis

Frontiers in Agronomy ◽

10.3389/fagro.2021.753474 ◽

2021 ◽

Vol 3 ◽

Author(s):

Calvin Cornell ◽

Vasilis Kokkoris ◽

Andrew Richards ◽

Christina Horst ◽

Daniel Rosa ◽

...

Keyword(s):

Microbial Diversity ◽

Microbial Communities ◽

Meta Analysis ◽

Soil Microbial Communities ◽

Sustainable Land Use ◽

Plant Performance ◽

Soil Microbiome ◽

Clear Understanding ◽

Soil Microbial Diversity ◽

Soil Microbial

There is a global industry built upon the production of “bioinoculants,” which include both bacteria and fungi. The recent increase in bioinoculant uptake by land users coincides with a drive for more sustainable land use practices. But are bioinoculants sustainable? These microbes are believed to improve plant performance, but knowledge of their effect on resident microbial communities is scant. Without a clear understanding of how they affect soil microbial communities (SMC), their utility is unclear. To assess how different inoculation practices may affect bioinoculant effects on SMC, we surveyed the existing literature. Our results show that bioinoculants significantly affect soil microbial diversity and that these effects are mediated by inoculant type, diversity, and disturbance regime. Further, these changes to soil microbes affect plant outcomes. Knowledge that these products may influence crop performance indirectly through changes to soil microbial diversity attests to the importance of considering the soil microbiome when assessing both bioinoculant efficacy and threats to soil ecosystems.

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Improvement of Soil Microbial Diversity through Sustainable Agricultural Practices and Its Evaluation by -Omics Approaches: A Perspective for the Environment, Food Quality and Human Safety

Microorganisms ◽

10.3390/microorganisms9071400 ◽

2021 ◽

Vol 9 (7) ◽

pp. 1400

Author(s):

Marta Bertola ◽

Andrea Ferrarini ◽

Giovanna Visioli

Keyword(s):

Microbial Diversity ◽

Food Quality ◽

Plant Biomass ◽

Soil Microbial Communities ◽

Well Being ◽

Plant Health ◽

Soil Microbiome ◽

Soil Microbial Diversity ◽

Soil Biodiversity ◽

Soil Microbial

Soil is one of the key elements for supporting life on Earth. It delivers multiple ecosystem services, which are provided by soil processes and functions performed by soil biodiversity. In particular, soil microbiome is one of the fundamental components in the sustainment of plant biomass production and plant health. Both targeted and untargeted management of soil microbial communities appear to be promising in the sustainable improvement of food crop yield, its nutritional quality and safety. –Omics approaches, which allow the assessment of microbial phylogenetic diversity and functional information, have increasingly been used in recent years to study changes in soil microbial diversity caused by agronomic practices and environmental factors. The application of these high-throughput technologies to the study of soil microbial diversity, plant health and the quality of derived raw materials will help strengthen the link between soil well-being, food quality, food safety and human health.

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Associations between human impacts and forest soil microbial communities

Elem Sci Anth ◽

10.1525/elementa.005 ◽

2020 ◽

Vol 8 (1) ◽

Author(s):

Yongjian Chen ◽

Jialiang Kuang ◽

Pandeng Wang ◽

Wensheng Shu ◽

Albert Barberán

Keyword(s):

Microbial Communities ◽

Forest Soil ◽

Human Activity ◽

Eastern China ◽

Soil Microbial Communities ◽

Nitrifying Bacteria ◽

Rrna Gene ◽

Internal Transcribed Spacer Region ◽

Soil Microbial ◽

Soil Variables

We are living in a new epoch—the Anthropocene, in which human activity is reshaping global biodiversity at an unprecedented rate. Increasing efforts are being made toward a better understanding of the associations between human activity and the geographic patterns in plant and animal communities. However, similar efforts are rarely applied to microbial communities. Here, we collected 472 forest soil samples across eastern China, and the bacterial and fungal communities in those samples were determined by high-throughput sequencing of 16S rRNA gene and internal transcribed spacer region, respectively. By compiling human impact variables as well as climate and soil variables, our goal was to elucidate the association between microbial richness and human activity when climate and soil variables are taken into account. We found that soil microbial richness was associated with human activity. Specifically, human population density was positively associated with the richness of bacteria, nitrifying bacteria and fungal plant pathogens, but it was negatively associated with the richness of cellulolytic bacteria and ectomycorrhizal fungi. Together, these results suggest that the associations between geographic variations of soil microbial richness and human activity still persist when climate and soil variables are taken into account and that these associations vary among different microbial taxonomic and functional groups.

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Dynamic Microbial Network Structure and Assembly Process in Rhizosphere and Bulk Soils Along a Coniferous Plantation Chronosequence

10.21203/rs.3.rs-1101835/v1 ◽

2021 ◽

Author(s):

Ying Wang ◽

Liguo Dong ◽

Min Zhang ◽

Xiaoxiong Bai ◽

Jiawen Zhang ◽

...

Keyword(s):

Total Phosphorus ◽

Fungal Community ◽

Soil Microbial Communities ◽

Dispersal Limitation ◽

Soil Samples ◽

Pinus Tabulaeformis ◽

Bulk Soil ◽

Microbial Composition ◽

Soil Microbial ◽

Plantation Development

Abstract Aims: During plantation development, microbial composition and diversity are critical for the establishment of plant diversity and multiple ecosystem functions. Here we aimed to evaluate the impacts of chronosequence and soil compartment on the bacterial and fungal community compositions, species co-occurrence, and assembly processes in forest ecosystem.Methods: Soils were collected in rhizosphere and bulk soils along a Pinus tabulaeformis plantation chronosequence (15, 30 and 60 years old). The bacterial and fungal communities were determined using amplicon sequencing.Results: The effect of stand age on the soil properties and microbial community structures was stronger than the effect of the soil compartment. In all soil samples, the dominant bacterial phyla were Proteobacteria, Acidobacteria, Actinobacteria, and Chloroflexi. Basidiomycota, Ascomycota, and Mortierellomycota were the dominant fungal phyla. Higher turnover rates of soil microbial communities were observed in rhizosphere soil than in bulk soil. Dispersal limitation governed the bacterial and fungal community assembly in all soil samples, and the fungal community was more susceptible to dispersal limitation. The bacterial and fungal keystone species compositions in the rhizosphere had significant positive correlations with the soil total phosphorus and nitrite nitrogen and total nitrogen and total phosphorus, respectively, indicating their importance in soil nitrogen and phosphorus cycling. The complexity of bacterial networks increased along the chronosequence. Fungal network complexity did not show a clear age-related trend but increased from bulk soil to the rhizosphere.Conclusions: During Pinus tabulaeformis plantation development, soil microbial assembly was less environmentally constrained due to an increase in resource availability.

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Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression

Microbiome ◽

10.1186/s40168-020-00892-z ◽

2020 ◽

Vol 8 (1) ◽

Cited By ~ 2

Author(s):

Chengyuan Tao ◽

Rong Li ◽

Wu Xiong ◽

Zongzhuan Shen ◽

Shanshan Liu ◽

...

Keyword(s):

Microbial Communities ◽

Plant Pathogens ◽

Organic Fertilizer ◽

Soil Microbial Communities ◽

Plant Diseases ◽

Disease Suppression ◽

Organic Fertilizers ◽

Soil Microbiome ◽

Soil Microbial ◽

Bioorganic Fertilizer

Abstract Background Plant diseases caused by fungal pathogen result in a substantial economic impact on the global food and fruit industry. Application of organic fertilizers supplemented with biocontrol microorganisms (i.e. bioorganic fertilizers) has been shown to improve resistance against plant pathogens at least in part due to impacts on the structure and function of the resident soil microbiome. However, it remains unclear whether such improvements are driven by the specific action of microbial inoculants, microbial populations naturally resident to the organic fertilizer or the physical-chemical properties of the compost substrate. The aim of this study was to seek the ecological mechanisms involved in the disease suppressive activity of bio-organic fertilizers. Results To disentangle the mechanism of bio-organic fertilizer action, we conducted an experiment tracking Fusarium wilt disease of banana and changes in soil microbial communities over three growth seasons in response to the following four treatments: bio-organic fertilizer (containing Bacillus amyloliquefaciens W19), organic fertilizer, sterilized organic fertilizer and sterilized organic fertilizer supplemented with B. amyloliquefaciens W19. We found that sterilized bioorganic fertilizer to which Bacillus was re-inoculated provided a similar degree of disease suppression as the non-sterilized bioorganic fertilizer across cropping seasons. We further observed that disease suppression in these treatments is linked to impacts on the resident soil microbial communities, specifically by leading to increases in specific Pseudomonas spp.. Observed correlations between Bacillus amendment and indigenous Pseudomonas spp. that might underlie pathogen suppression were further studied in laboratory and pot experiments. These studies revealed that specific bacterial taxa synergistically increase biofilm formation and likely acted as a plant-beneficial consortium against the pathogen. Conclusion Together we demonstrate that the action of bioorganic fertilizer is a product of the biocontrol inoculum within the organic amendment and its impact on the resident soil microbiome. This knowledge should help in the design of more efficient biofertilizers designed to promote soil function.

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Visualizing Microbial Community Dynamics via a Controllable Soil Environment

mSystems ◽

10.1128/msystems.00645-19 ◽

2020 ◽

Vol 5 (1) ◽

Cited By ~ 1

Author(s):

Arunima Bhattacharjee ◽

Dusan Velickovic ◽

Thomas W. Wietsma ◽

Sheryl L. Bell ◽

Janet K. Jansson ◽

...

Keyword(s):

Soil Moisture ◽

Microbial Community ◽

Microbial Communities ◽

Community Dynamics ◽

Soil Microbial Communities ◽

Soil Microbiome ◽

Soil Core ◽

Soil Microbial ◽

Functional Relationships ◽

Microbial Community Dynamics

ABSTRACT Understanding the basic biology that underpins soil microbiome interactions is required to predict the metaphenomic response to environmental shifts. A significant knowledge gap remains in how such changes affect microbial community dynamics and their metabolic landscape at microbially relevant spatial scales. Using a custom-built SoilBox system, here we demonstrated changes in microbial community growth and composition in different soil environments (14%, 24%, and 34% soil moisture), contingent upon access to reservoirs of nutrient sources. The SoilBox emulates the probing depth of a common soil core and enables determination of both the spatial organization of the microbial communities and their metabolites, as shown by confocal microscopy in combination with mass spectrometry imaging (MSI). Using chitin as a nutrient source, we used the SoilBox system to observe increased adhesion of microbial biomass on chitin islands resulting in degradation of chitin into N-acetylglucosamine (NAG) and chitobiose. With matrix-assisted laser desorption/ionization (MALDI)-MSI, we also observed several phospholipid families that are functional biomarkers for microbial growth on the chitin islands. Fungal hyphal networks bridging different chitin islands over distances of 27 mm were observed only in the 14% soil moisture regime, indicating that such bridges may act as nutrient highways under drought conditions. In total, these results illustrate a system that can provide unprecedented spatial information about interactions within soil microbial communities as a function of changing environments. We anticipate that this platform will be invaluable in spatially probing specific intra- and interkingdom functional relationships of microbiomes within soil. IMPORTANCE Microbial communities are key components of the soil ecosystem. Recent advances in metagenomics and other omics capabilities have expanded our ability to characterize the composition and function of the soil microbiome. However, characterizing the spatial metabolic and morphological diversity of microbial communities remains a challenge due to the dynamic and complex nature of soil microenvironments. The SoilBox system, demonstrated in this work, simulates an ∼12-cm soil depth, similar to a typical soil core, and provides a platform that facilitates imaging the molecular and topographical landscape of soil microbial communities as a function of environmental gradients. Moreover, the nondestructive harvesting of soil microbial communities for the imaging experiments can enable simultaneous multiomics analysis throughout the depth of the SoilBox. Our results show that by correlating molecular and optical imaging data obtained using the SoilBox platform, deeper insights into the nature of specific soil microbial interactions can be achieved.

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