Iron mineralogy and uranium-binding environment in the rhizosphere of a wetland soil
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Kaplan, Daniel I.↗
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The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies
Over the past century, the significance of the rhizosphere as a complex, biological system, comprised of vast, interconnected networks of microbial organisms that interact directly with their plant hosts (e.g., archæa, bacteria, fungi, eukaryotes, and viruses) has been increasingly recognized by the scientific community. Providing a nutritional base to the terrestrial biosphere, the rhizosphere is integral to plant growth, crop production and ecosystem health. Lack of mechanistic understanding of the rhizosphere constitutes a critical knowledge gap, inhibiting our ability to predict and control the terrestrial ecosystem in order to achieve desirable outcomes (e.g., bioenergy production, crop yield maximization, and soilbased carbon sequestration). Application of multi-omics has the potential to significantly advance our knowledge of rhizospheric science. This review covers: cutting- and bleeding-edge, multi-omic techniques and technologies; methods and protocols for specific rhizospheric science questions; and, challenges to be addressed during this century of rhizospheric science.
multi-omics↗
New understanding of rhizosphere processes enabled by advances in molecular and spatially resolved techniques
Understanding the role played by microorganisms within soil systems is challenged by the unique intersection of physics, chemistry, mineralogy and biology in fostering habitat for soil microbial communities. To address these challenges will require observations across multiple spatial and temporal scales to capture the dynamics and emergent behavior from complex and interdependent processes. The heterogeneity and complexity of the rhizosphere require advanced techniques that press the simultaneous frontiers of spatial resolution, analyte sensitivity and specificity, reproducibility, large dynamic range, and high throughput. Fortunately many exciting technical advancements are now available to inform and guide the development of new hypotheses. The aim of this Special issue is to provide a holistic view of the rhizosphere in the perspective of modern molecular biology methodologies that enabled a highly-focused, detailed view on the processes in the rhizosphere, including numerous, strong and complex interactions between plant roots, soil constituents and microorganisms. We discuss the current rhizosphere research challenges and knowledge gaps, as well as perspectives and approaches using newly available state-of-the-art toolboxes. These new approaches and methodologies allow the study of rhizosphere processes and properties, and rhizosphere as a central component of ecosystems and biogeochemical cycles.
Holistic view↗
Predicting Ecological Roles in the Rhizosphere Using Metabolome and Transportome Modeling
The ability to obtain complete genome sequences from bacteria in environmental samples, such as soil samples from the rhizosphere, has highlighted the microbial diversity and complexity of environmental communities. However, new algorithms to analyze genome sequence information in the context of community structure are needed to enhance our understanding of the specific ecological roles of these organisms in soil environments. We present a machine learning approach using sequenced Pseudomonad genomes coupled with outputs of metabolic and transportomic computational models for identifying the most predictive molecular mechanisms indicative of a Pseudomonad's ecological role in the rhizosphere: a biofilm, biocontrol agent, promoter of plant growth, or plant pathogen. Computational predictions of ecological niche were highly accurate overall with models trained on transportomic model output being the most accurate (Leave One Out Validation F-scores between 0.82 and 0.89). The strongest predictive molecular mechanism features for rhizosphere ecological niche overlap with many previously reported analyses of Pseudomonad interactions in the rhizosphere, suggesting that this approach successfully informs a system-scale level understanding of how Pseudomonads sense and interact with their environments. The observation that an organism's transportome is highly predictive of its ecological niche is a novel discovery and may have implications in our understanding microbial ecology. The framework developed here can be generalized to the analysis of any bacteria across a wide range of environments and ecological niches making this approach a powerful tool for providing insights into functional predictions from bacterial genomic data.
59 BASIC BIOLOGICAL SCIENCES↗
Mass spectrometry imaging: Towards mapping the elemental and molecular composition of the rhizosphere
This short review will discuss and provide perspective into the utilization of mass spectrometry imaging (MSI) in studying the rhizosphere. It also serves to compliment the multi-omic focused review by White et al. in this journal issue, as MSI is capable of elucidating chemical distributions within samples of interest in an in situ fashions, and thus can provide spatial context to MS omics data in complementary experimental endeavors. The majority of reported MSI-based studies of plant-microbe interactions have focused on the phyllosphere and ‘associated rhizosphere’ (e.g., material that is not removed during harvesting), as sample preparation for these in situ analyses tends to be a limiting factor. These studies have provided valuable insight into the spatial arrangement of proteins, peptides, lipids, and other metabolites within these systems. We intend for this short review to be a primer about the history of MSI and its role in plant-microbe analysis. Along the way we reference many comprehensive reviews for the interested reader. Lastly, we offer a perspective on the future of MSI and its use in understanding the molecular transformations beyond what we coined as the ‘associated rhizosphere’ to the rest of rhizosphere zone and into the bulk soil.
54 ENVIRONMENTAL SCIENCES↗
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
While interactions between roots and microorganisms have been intensively studied, we know little about interactions among root-associated microbes. We used random matrix theory-based network analysis of 16S rRNA genes to identify bacterial networks associated with wild oat (Avena fatua) over two seasons in greenhouse microcosms. Rhizosphere networks were substantially more complex than those in surrounding soils, indicating the rhizosphere has a greater potential for interactions and niche-sharing. Network complexity increased as plants grew, even as diversity decreased, highlighting that community organisation is not captured by univariate diversity. Covariations were predominantly positive (> 80%), suggesting that extensive mutualistic interactions may occur among rhizosphere bacteria; we identified quorum-based signalling as one potential strategy. Putative keystone taxa often had low relative abundances, suggesting low-abundance taxa may significantly contribute to rhizosphere function. Network complexity, a previously undescribed property of the rhizosphere microbiome, appears to be a defining characteristic of this habitat.
54 ENVIRONMENTAL SCIENCES↗
Below-ground connections underlying above-ground food production: a framework for optimising ecological connections in the rhizosphere
Not provided.
Environmental Sciences & Ecology↗
Optimized CRISPR Interference System for Investigating Pseudomonas alloputida Genes Involved in Rhizosphere Microbiome Assembly
Pseudomonas alloputida KT2440 (formerly P. putida) has become both a well-known chassis organism for synthetic biology and a model organism for rhizosphere colonization. Here, we describe a CRISPR interference (CRISPRi) system in KT2440 for exploring microbe–microbe interactions in the rhizosphere and for use in industrial systems. Our CRISPRi system features three different promoter systems (XylS/P m , LacI/P lac , and AraC/P BAD ) and a dCas9 codon-optimized for Pseudomonads, all located on a mini-Tn7-based transposon that inserts into a neutral site in the genome. It also includes a suite of pSEVA-derived sgRNA expression vectors, where the expression is driven by synthetic promoters varying in strength. We compare the three promoter systems in terms of how well they can precisely modulate gene expression, and we discuss the impact of environmental factors, such as media choice, on the success of CRISPRi. We demonstrate that CRISPRi is functional in bacteria colonizing the rhizosphere, with repression of essential genes leading to a 10–100-fold reduction in P. alloputida cells per root. Finally, we show that CRISPRi can be used to modulate microbe–microbe interactions. When the gene pvdH is repressed and P. alloputida is unable to produce pyoverdine, it loses its ability to inhibit other microbes in vitro. Furthermore, our design is amendable for future CRISPRi-seq studies and in multispecies microbial communities, with the different promoter systems providing a means to control the level of gene expression in many different environments.
Bacteria↗
Feedbacks between plant N demand and rhizosphere priming depend on type of mycorrhizal association
Not provided.
Environmental Sciences & Ecology↗
Using Raman spectroscopy and SERS for in situ studies of rhizosphere bacteria
need
22 GENERAL STUDIES OF NUCLEAR REACTORS↗
Assessment of rhizosphere bacterial diversity and composition in a metal hyperaccumulator (Boehmeria nivea) and a nonaccumulator (Artemisia annua) in an antimony mine
Abstract Aims Heavy metal hyperaccumulators are widely used in mining restoration due to their ability to accumulate and transport heavy metals, compared to nonaccumulators. Rhizosphere bacteria in metal hyperaccumulators play a key role in the uptake of heavy metals from soil; however, assessments of the differences of rhizosphere bacteria between metal hyperaccumulators and nonaccumulator are scarce. Methods and results To understand the difference of bacterial composition between hyperaccumulator and nonaccumulator in rhizosphere, the diversity and composition of rhizosphere bacteria in a metal hyperaccumulator (Boehmeria nivea) and a nonaccumulator (Artemisia annua) grown in the same field in Xikuangshan were evaluated using Illumina Miseq high-throughput sequencing technology. Boehmeria nivea and A. annua had 3926 overlapping OTUs, 19,736 and 17,579 unique OTUs, respectively. Boehmeria nivea had lower Chao1 index, Shannon index and Pielou index than A. annua. The dominant phyla and genera of rhizosphere bacteria in B. nivea and A. annua were similar, but some rhizosphere bacterial communities with heavy metal remediation ability mainly appeared in the rhizosphere of the hyperaccumulator. Compared to A. annua, B. nivea showed a significantly higher relative abundance of rhizosphere bacteria, such as Acidobacteria and Bacteroidete at the phylum level and RB41 at the genus level. Some specific rhizosphere bacteria with the ability to bind metal, such as Leifsonia and Kibdelosporangium, were only found in the rhizosphere of B. nivea. Conclusion Results indicated that B. nivea, as a metal hyperaccumulator, has a key function in governing metal-resistant rhizosphere bacteria in response to antimony compound pollution stress. Significance and Impact of Study Understanding the diversity of rhizosphere bacteria between hyperaccumulators and nonaccumulators is beneficial to formulate strategies to improve metal uptake efficiency by selecting specific plant species and rhizosphere bacteria grown on polluted soil.
Lin, Yuxiang↗
Successional trajectories of rhizosphere bacterial communities over consecutive seasons
It is well known that rhizosphere microbiomes differ from those of surrounding soil, and yet we know little about how these root-associated microbial communities change through the growing season and between seasons. We analyzed the response of soil bacteria to roots of the common annual grass Avena fatua over two growing seasons using high-throughput sequencing of 16S rRNA genes. Over the two periods of growth, the rhizosphere bacterial communities followed consistent successional patterns as plants grew, although the starting communities were distinct. Succession in the rhizosphere was characterized by a significant decrease in both taxonomic and phylogenetic diversity relative to background soil communities, driven by reductions in both richness and evenness of the bacterial communities. Plant roots selectively stimulated the relative abundance of Alphaproteobacteria , Betaproteobacteria , and Bacteroidetes but reduced the abundance of Acidobacteria , Actinobacteria , and Firmicutes . Taxa that increased in relative abundance in the rhizosphere soil displayed phylogenetic clustering, suggesting some conservation and an evolutionary basis for the response of complex soil bacterial communities to the presence of plant roots. The reproducibility of rhizosphere succession and the apparent phylogenetic conservation of rhizosphere competence traits suggest adaptation of the indigenous bacterial community to this common grass over the many decades of its presence. We document the successional patterns of rhizosphere bacterial communities associated with a “wild” annual grass, Avena fatua , which is commonly a dominant plant in Mediterranean-type annual grasslands around the world; the plant was grown in its grassland soil. Most studies documenting rhizosphere microbiomes address “domesticated” plants growing in soils to which they are introduced. Rhizosphere bacterial communities exhibited a pattern of temporal succession that was consistent and repeatable over two growing seasons. There are few studies assessing the reproducibility over multiple seasons. Through the growing season, the rhizosphere community became progressively less diverse, likely reflecting root homogenization of soil microniches. Phylogenetic clustering of the rhizosphere dynamic taxa suggests evolutionary adaptation to Avena roots. The reproducibility of rhizosphere succession and the apparent phylogenetic conservation of rhizosphere competence traits suggest adaptation of the indigenous bacterial community to this common grass over the many decades of its presence.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
Abstract Background Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues to grow, but there remains a need to understand the extent to which biological and environmental factors mediate protist community assembly and dynamics. We hypothesize that protists communities are filtered by the influence of plants on their rhizosphere biological and physicochemical environment, resulting in patterns of protist diversity and composition that mirror previously observed diversity and successional dynamics in rhizosphere bacterial communities. Results We analyzed protist communities associated with the rhizosphere and bulk soil of switchgrass (SG) plants ( Panicum virgatum ) at different phenological stages, grown in two marginal soils as part of a large-scale field experiment. Our results reveal that the diversity of protists is lower in rhizosphere than bulk soils, and that temporal variations depend on soil properties but are less pronounced in rhizosphere soil. Patterns of significantly prevalent protists groups in the rhizosphere suggest that most protists play varied ecological roles across plant growth stages and that some plant pathogenic protists and protists with omnivorous diets reoccur over time in the rhizosphere. We found that protist co-occurrence network dynamics are more complex in the rhizosphere compared to bulk soil. A phylogenetic bin-based null model analysis showed that protists’ community assembly in our study sites is mainly controlled by homogenous selection and dispersal limitation, with stronger selection in rhizosphere than bulk soil as SG grew and senesced. Conclusions We demonstrate that environmental filtering is a dominant determinant of overall protist community properties and that at the rhizosphere level, plant control on the physical and biological environment is a critical driver of protist community composition and dynamics. Since protists are key contributors to plant nutrient availability and bacterial community composition and abundance, mapping and understanding their patterns in rhizosphere soil is foundational to understanding the ecology of the root-microbe-soil system.
54 ENVIRONMENTAL SCIENCES↗
From data to knowledge: The future of multi-omics data analysis for the rhizosphere
The rhizosphere is the interface between the root system of a plant and its surrounding soil. The microbiome of the rhizosphere, which is the totality of all microbes present there, represents a complex microbial ecosystem that nourishes the terrestrial biosphere. In order to untangle the complexity of the rhizosphere, and of the rhizospheric microbiome in particular, an integrated multi-omics approach can be applied to reveal the composition of the rhizospheric microbiome (through 16S ribosomal amplicons and metagenomics), the functional properties of the microbiome (through metatranscriptomics and metaproteomics), and the signaling network within the rhizosphere (through metametabolomics). The successful application of integrated multi-omics to rhizospheric science depends on the availability of rhizosphere-specific data and on the appropriate software used to analyze omics data from the rhizosphere. Here, we analyze the availability of software suites that are normally applied to surrogate disciplines (e.g., soil and plants) but which can be used for rhizospheric science. We also identify potential issues, challenges, and opportunities for rhizosphere science.
54 ENVIRONMENTAL SCIENCES↗
Assessing horizontal gene transfer in the rhizosphere of Brachypodium distachyon using fabricated ecosystems (EcoFABs)
ABSTRACT Horizontal gene transfer (HGT) is a major process by which genes are transferred between microbes in the rhizosphere. However, examining HGT remains challenging due to the complexity of mimicking conditions within the rhizosphere. Fabricated ecosystems (EcoFABs) have been used to investigate several complex processes in plant-associated environments. Here we show that EcoFABs are efficient tools to examine and measure HGT frequency in the rhizosphere. We provide the first demonstration of gene transfer via a triparental conjugation system in the Brachypodium distachyon rhizosphere in an EcoFAB using Pseudomonas putida KT2440 as both donor and recipient bacterial strain with the donor containing a mobilizable and non-self-transmissible plasmid. We observed that the frequency of plasmid transfer in the rhizosphere is potentially dependent on the plant developmental stage and the composition and amount of root exudates. The frequency of plasmid transfer also increased with higher numbers of donor cells. We demonstrate the transfer of plasmid from P. putida to another B. distachyon root colonizer, Burkholderia sp. OAS925, showing HGT within a rhizosphere microbial community. Environmental stresses also influenced the rate and efficiency of HGT in the rhizosphere between different species and genera. This study provides a robust workflow to evaluate transfer of engineered plasmids in the rhizosphere when such plasmids are potentially introduced in a field or other plant-associated environments. IMPORTANCE We report the use of EcoFABs to investigate the HGT process in a rhizosphere environment. It highlights the potential of EcoFABs in recapitulating the dynamic rhizosphere conditions as well as their versatility in studying plant-microbe interactions. This study also emphasizes the importance of studying the parameters impacting the HGT frequency. Several factors such as plant developmental stages, nutrient conditions, number of donor cells, and environmental stresses influence gene transfer within the rhizosphere microbial community. This study paves the way for future investigations into understanding the fate and movement of engineered plasmids in a field environment.
Priya, Shweta↗
Uncovering the dominant role of root metabolism in shaping rhizosphere metabolome under drought in tropical rainforest plants
Plant-soil-microbe interactions are crucial for driving rhizosphere processes that contribute to metabolite turnover and nutrient cycling. With the increasing frequency and severity of water scarcity due to climate warming, understanding how plant-mediated processes, such as root exudation, influence soil organic matter turnover in the rhizosphere is essential. In this study, we used 16S rRNA gene amplicon sequencing, rhizosphere metabolomics, and position-specific 13 C-pyruvate labeling to examine the effects of three different plant species (Piper auritum, Hibiscus rosa sinensis, and Clitoria fairchildiana) and their associated microbial communities on soil organic carbon turnover in the rhizosphere. Here, our findings indicate that in these tropical plants, the rhizosphere metabolome is primarily shaped by the response of roots to drought rather than direct shifts in the rhizosphere bacterial community composition. Specifically, the reduced exudation of plant roots had a notable effect on the metabolome of the rhizosphere of P. auritum, with less reliance on neighboring microbes. Contrary to P. auritum, H. rosa sinensis and C. fairchildiana experienced changes in their exudate composition during drought, causing alterations to the bacterial communities in the rhizosphere. This, in turn, had a collective impact on the rhizosphere's metabolome. Furthermore, the exclusion of phylogenetically distant microbes from the rhizosphere led to shifts in its metabolome. Additionally, C. fairchildiana appeared to be associated with only a subset of symbiotic bacteria under drought conditions. These results indicate that plant species-specific microbial interactions systematically change with the root metabolome. As roots respond to drought, their associated microbial communities adapt, potentially reinforcing the drought tolerance strategies of plant roots. These findings have significant implications for maintaining plant health and preference during drought stress and improving plant performance under climate change.
54 ENVIRONMENTAL SCIENCES↗
Nutrient and moisture limitations reveal keystone metabolites linking rhizosphere metabolomes and microbiomes
Plants release a wealth of metabolites into the rhizosphere that can shape the composition and activity of microbial communities in response to environmental stress. The connection between rhizodeposition and rhizosphere microbiome succession has been suggested, particularly under environmental stress conditions, yet definitive evidence is scarce. In this study, we investigated the relationship between rhizosphere chemistry, microbiome dynamics, and abiotic stress in the bioenergy crop switchgrass grown in a marginal soil under nutrient-limited, moisture-limited, and nitrogen (N)-replete, phosphorus (P)-replete, and NP-replete conditions. We combined 16S rRNA amplicon sequencing and LC-MS/MS-based metabolomics to link rhizosphere microbial communities and metabolites. We identified significant changes in rhizosphere metabolite profiles in response to abiotic stress and linked them to changes in microbial communities using network analysis. N-limitation amplified the abundance of aromatic acids, pentoses, and their derivatives in the rhizosphere, and their enhanced availability was linked to the abundance of bacterial lineages from Acidobacteria, Verrucomicrobia, Planctomycetes, and Alphaproteobacteria. Conversely, N-amended conditions increased the availability of N-rich rhizosphere compounds, which coincided with proliferation of Actinobacteria. Treatments with contrasting N availability differed greatly in the abundance of potential keystone metabolites; serotonin and ectoine were particularly abundant in N-replete soils, while chlorogenic, cinnamic, and glucuronic acids were enriched in N-limited soils. Serotonin, the keystone metabolite we identified with the largest number of links to microbial taxa, significantly affected root architecture and growth of rhizosphere microorganisms, highlighting its potential to shape microbial community and mediate rhizosphere plant–microbe interactions.
59 BASIC BIOLOGICAL SCIENCES↗