Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes.

Plant roots support complex microbial communities that can influence plant growth, nutrition, and health. While extensive characterizations of the composition and spatial compartmentalization of these communities have been performed in different plant species, there is relatively little known about the impact of abiotic stresses on the root microbiota. Here, we have used rice as a model to explore the responses of root microbiomes to drought stress. Using four distinct genotypes, grown in soils from three different fields, we tracked the drought-induced changes in microbial composition in the rhizosphere (the soil immediately surrounding the root), the endosphere (the root interior), and unplanted soils. Drought significantly altered the overall bacterial and fungal compositions of all three communities, with the endosphere and rhizosphere compartments showing the greatest divergence from well-watered controls. The overall response of the bacterial microbiota to drought stress was taxonomically consistent across soils and cultivars and was primarily driven by an enrichment of multiple Actinobacteria and Chloroflexi, as well as a depletion of several Acidobacteria and Deltaproteobacteria While there was some overlap in the changes observed in the rhizosphere and endosphere communities, several drought-responsive taxa were compartment specific, a pattern likely arising from preexisting compositional differences, as well as plant-mediated processes affecting individual compartments. These results reveal that drought stress, in addition to its well-characterized effects on plant physiology, also results in restructuring of root microbial communities and suggest the possibility that constituents of the altered plant microbiota might contribute to plant survival under extreme environmental conditions.IMPORTANCE With the likelihood that changes in global climate will adversely affect crop yields, the potential role of microbial communities in enhancing plant performance makes it important to elucidate the responses of plant microbiomes to environmental variation. By detailed characterization of the effect of drought stress on the root-associated microbiota of the crop plant rice, we show that the rhizosphere and endosphere communities undergo major compositional changes that involve shifts in the relative abundances of a taxonomically diverse set of bacteria in response to drought. These drought-responsive microbes, in particular those enriched under water deficit conditions, could potentially benefit the plant as they could contribute to tolerance to drought and other abiotic stresses, as well as provide protection from opportunistic infection by pathogenic microbes. The identification and future isolation of microbes that promote plant tolerance to drought could potentially be used to mitigate crop losses arising from adverse shifts in climate

Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters.

Rice cultivation worldwide accounts for ∼7 to 17% of global methane emissions. Methane cycling in rice paddies is a microbial process not only involving methane producers (methanogens) and methane metabolizers (methanotrophs) but also other microbial taxa that affect upstream processes related to methane metabolism. Rice cultivars vary in their rates of methane emissions, but the influence of rice genotypes on methane cycling microbiota has been poorly characterized. Here, we profiled the rhizosphere, rhizoplane, and endosphere microbiomes of a high-methane-emitting cultivar (Sabine) and a low-methane-emitting cultivar (CLXL745) throughout the growing season to identify variations in the archaeal and bacterial communities relating to methane emissions. The rhizosphere of the high-emitting cultivar was enriched in methanogens compared to that in the low emitter, whereas the relative abundances of methanotrophs between the cultivars were not significantly different. Further analysis of cultivar-sensitive taxa identified families enriched in the high emitter that are associated with methanogenesis-related processes. The high emitter had greater relative abundances of sulfate-reducing and iron-reducing taxa which peak earlier in the season than methanogens and are necessary to lower soil oxidation reduction potential before methanogenesis can occur. The high emitter also had a greater abundance of fermentative taxa which produce methanogenesis precursors (acetate, CO2, and H2). Furthermore, the high emitter was enriched in taxa related to acetogenesis which compete with methanogens for CO2 and H2 These taxa were enriched in a spatio-specific manner and reveal a complex network of microbial interactions on which plant genotype-dependent factors can act to affect methanogenesis and methane emissions.IMPORTANCE Rice cultivation is a major source of anthropogenic emissions of methane, a greenhouse gas with a potentially severe impact on climate change. Emission variation between rice cultivars suggests the feasibility of breeding low-emission rice, but there is a limited understanding of how genotypes affect the microbiota involved in methane cycling. Here, we show that the root microbiome of the high-emitting cultivar is enriched both in methanogens and in taxa associated with fermentation, iron, and sulfate reduction and acetogenesis, processes that support methanogenesis. Understanding how cultivars affect microbes with methanogenesis-related functions is vital for understanding the genetic basis for methane emission in rice and can aid in the development of breeding programs that reduce the environmental impact of rice cultivation

Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota.

BackgroundSoils are a key component of agricultural productivity, and soil microbiota determine the availability of many essential plant nutrients. Agricultural domestication of soils, that is, the conversion of previously uncultivated soils to a cultivated state, is frequently accompanied by intensive monoculture, especially in the developing world. However, there is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domestication, including to what extent crop plants impact soil microbiota composition, and how changes in microbiota composition arising from cultivation affect crop performance.ResultsWe show here that continuous monoculture (> 8 growing seasons) of the major food crop rice under flooded conditions is associated with a pronounced shift in soil bacterial and archaeal microbiota structure towards a more consistent composition, thereby domesticating microbiota of previously uncultivated sites. Aside from the potential effects of agricultural cultivation practices, we provide evidence that rice plants themselves are important drivers of the domestication process, acting through selective enrichment of specific taxa, including methanogenic archaea, in their rhizosphere that differ from those of native plants growing in the same environment. Furthermore, we find that microbiota from soils domesticated by rice cultivation contribute to plant-soil feedback, by imparting a negative effect on rice seedling vigor.ConclusionsSoil domestication through continuous monoculture cultivation of rice results in compositional changes in the soil microbiota, which are in part driven by the rice plants. The consequences include a negative impact on plant performance and increases in greenhouse gas emitting microbes

Taxonomies, Functions, and Applications of Rice-Associated Microbiome

Plant-associated microbes form complex interactions within their microbial community as well as with the host, affecting processes such as nutrient and carbon cycling, abiotic stress protection, and disease resistance. Understanding the interactions of the host and host-associated microbiomes could potentially aid plant health in a variety of ways and is therefore of interest to the plant science community. Rice is a unique system to study plant-microbe interactions because of flooded conditions in which it is cultivated. This anoxic environment leads to a host of anaerobic microbial taxa associating with the rice host which harbor functions dependent on the anoxic conditions, including methanogenesis. In this thesis, I describe three studies where we profile the taxonomies and functions of rice-associated microbiomes and demonstrate how the knowledge gained from these methods can be applied in discovering microbial isolates that are beneficial to the plant host.In the first chapter, I present a study that characterizes the microbiomes of a high- and a low-methane-emitting rice cultivar throughout the growing season. We found that the high methane emitting cultivar had a higher relative abundance of methanogenic archaea in the rhizosphere, and additionally had a greater abundance of taxa associated with fermentation, which could be responsible for producing methanogenic precursor molecules. In the second chapter, I present a study that characterizes the effects of drought and recovery on the microbiome. We found that a Streptomyces taxa became the most abundant member of the endosphere community during and after drought, and that this member was prevalent in rice samples from various locations. We cultured a corresponding isolate and demonstrated that it had similar qualities to the Streptomyces from the study (it was endophytic and increased in relative abundance under drought stress) and promoted root growth, demonstrating the enrichment of this microbe under drought could potentially mitigate drought effects. In the third chapter, I present a study demonstrating the effects of nitrogen on the microbiome in three different soils by profiling both the taxonomies and functions through genome-resolved metagenomics. We found that the response of rice-associated microbiomes to the nitrogen fertilizer was largely soil specific, though there were general increases in Gammaproteobacteria and decreases in Actinobacteria in response to nitrogen. Profiling the metagenome demonstrated that nitrogen fertilizer increased the abundance of genes related to aromatic compound degradation, fermentation, and methanogenesis. We also recovered 60 metagenome assembled genomes, which to our knowledge is the first such dataset of its kind in rice, and can be a valuable resource to further understanding the dynamics of microbes associating with rice

Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes.

Plant roots support complex microbial communities that can influence plant growth, nutrition, and health. While extensive characterizations of the composition and spatial compartmentalization of these communities have been performed in different plant species, there is relatively little known about the impact of abiotic stresses on the root microbiota. Here, we have used rice as a model to explore the responses of root microbiomes to drought stress. Using four distinct genotypes, grown in soils from three different fields, we tracked the drought-induced changes in microbial composition in the rhizosphere (the soil immediately surrounding the root), the endosphere (the root interior), and unplanted soils. Drought significantly altered the overall bacterial and fungal compositions of all three communities, with the endosphere and rhizosphere compartments showing the greatest divergence from well-watered controls. The overall response of the bacterial microbiota to drought stress was taxonomically consistent across soils and cultivars and was primarily driven by an enrichment of multiple Actinobacteria and Chloroflexi, as well as a depletion of several Acidobacteria and Deltaproteobacteria While there was some overlap in the changes observed in the rhizosphere and endosphere communities, several drought-responsive taxa were compartment specific, a pattern likely arising from preexisting compositional differences, as well as plant-mediated processes affecting individual compartments. These results reveal that drought stress, in addition to its well-characterized effects on plant physiology, also results in restructuring of root microbial communities and suggest the possibility that constituents of the altered plant microbiota might contribute to plant survival under extreme environmental conditions.IMPORTANCE With the likelihood that changes in global climate will adversely affect crop yields, the potential role of microbial communities in enhancing plant performance makes it important to elucidate the responses of plant microbiomes to environmental variation. By detailed characterization of the effect of drought stress on the root-associated microbiota of the crop plant rice, we show that the rhizosphere and endosphere communities undergo major compositional changes that involve shifts in the relative abundances of a taxonomically diverse set of bacteria in response to drought. These drought-responsive microbes, in particular those enriched under water deficit conditions, could potentially benefit the plant as they could contribute to tolerance to drought and other abiotic stresses, as well as provide protection from opportunistic infection by pathogenic microbes. The identification and future isolation of microbes that promote plant tolerance to drought could potentially be used to mitigate crop losses arising from adverse shifts in climate

Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters.

Rice cultivation worldwide accounts for ∼7 to 17% of global methane emissions. Methane cycling in rice paddies is a microbial process not only involving methane producers (methanogens) and methane metabolizers (methanotrophs) but also other microbial taxa that affect upstream processes related to methane metabolism. Rice cultivars vary in their rates of methane emissions, but the influence of rice genotypes on methane cycling microbiota has been poorly characterized. Here, we profiled the rhizosphere, rhizoplane, and endosphere microbiomes of a high-methane-emitting cultivar (Sabine) and a low-methane-emitting cultivar (CLXL745) throughout the growing season to identify variations in the archaeal and bacterial communities relating to methane emissions. The rhizosphere of the high-emitting cultivar was enriched in methanogens compared to that in the low emitter, whereas the relative abundances of methanotrophs between the cultivars were not significantly different. Further analysis of cultivar-sensitive taxa identified families enriched in the high emitter that are associated with methanogenesis-related processes. The high emitter had greater relative abundances of sulfate-reducing and iron-reducing taxa which peak earlier in the season than methanogens and are necessary to lower soil oxidation reduction potential before methanogenesis can occur. The high emitter also had a greater abundance of fermentative taxa which produce methanogenesis precursors (acetate, CO2, and H2). Furthermore, the high emitter was enriched in taxa related to acetogenesis which compete with methanogens for CO2 and H2 These taxa were enriched in a spatio-specific manner and reveal a complex network of microbial interactions on which plant genotype-dependent factors can act to affect methanogenesis and methane emissions.IMPORTANCE Rice cultivation is a major source of anthropogenic emissions of methane, a greenhouse gas with a potentially severe impact on climate change. Emission variation between rice cultivars suggests the feasibility of breeding low-emission rice, but there is a limited understanding of how genotypes affect the microbiota involved in methane cycling. Here, we show that the root microbiome of the high-emitting cultivar is enriched both in methanogens and in taxa associated with fermentation, iron, and sulfate reduction and acetogenesis, processes that support methanogenesis. Understanding how cultivars affect microbes with methanogenesis-related functions is vital for understanding the genetic basis for methane emission in rice and can aid in the development of breeding programs that reduce the environmental impact of rice cultivation

Data from: Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life-cycle in field-grown rice

Bacterial communities associated with roots impact the health and nutrition of the host plant. The dynamics of these microbial assemblies over the plant life cycle is however, not well understood. Here, we use dense temporal sampling of 1588 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of three consecutive growing seasons, as well as two sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth, then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forests approach. The age-prediction models revealed that drought stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle

Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice.

Bacterial communities associated with roots impact the health and nutrition of the host plant. The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of 3 consecutive growing seasons, as well as 2 sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth and then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forest approach. The age-prediction models revealed that drought-stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle