skip to main content


Title: Pseudomonas cultivated from Andropogon gerardii rhizosphere show functional potential for promoting plant host growth and drought resilience
Abstract Background

Climate change will result in more frequent droughts that can impact soil-inhabiting microbiomes (rhizobiomes) in the agriculturally vital North American perennial grasslands. Rhizobiomes have contributed to enhancing drought resilience and stress resistance properties in plant hosts. In the predicted events of more future droughts, how the changing rhizobiome under environmental stress can impact the plant host resilience needs to be deciphered. There is also an urgent need to identify and recover candidate microorganisms along with their functions, involved in enhancing plant resilience, enabling the successful development of synthetic communities.

Results

In this study, we used the combination of cultivation and high-resolution genomic sequencing of bacterial communities recovered from the rhizosphere of a tallgrass prairie foundation grass,Andropogon gerardii. We cultivated the plant host-associated microbes under artificial drought-induced conditions and identified the microbe(s) that might play a significant role in the rhizobiome ofAndropogon gerardiiunder drought conditions. Phylogenetic analysis of the non-redundant metagenome-assembled genomes (MAGs) identified a bacterial genome of interest – MAG-Pseudomonas. Further metabolic pathway and pangenome analyses recovered genes and pathways related to stress responses including ACC deaminase; nitrogen transformation including assimilatory nitrate reductase in MAG-Pseudomonas,which might be associated with enhanced drought tolerance and growth forAndropogon gerardii.

Conclusions

Our data indicated that the metagenome-assembled MAG-Pseudomonashas the functional potential to contribute to the plant host’s growth during stressful conditions. Our study also suggested the nitrogen transformation potential ofMAG-Pseudomonasthat could impactAndropogon gerardiigrowth in a positive way. The cultivation of MAG-Pseudomonassets the foundation to construct a successful synthetic community forAndropogon gerardii. To conclude, stress resilience mediated through genes ACC deaminase, nitrogen transformation potential through assimilatory nitrate reductase in MAG-Pseudomonascould place this microorganism as an important candidate of the rhizobiome aiding the plant host resilience under environmental stress. This study, therefore, provided insights into the MAG-Pseudomonasand its potential to optimize plant productivity under ever-changing climatic patterns, especially in frequent drought conditions.

 
more » « less
NSF-PAR ID:
10383030
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
BMC Genomics
Volume:
23
Issue:
1
ISSN:
1471-2164
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Arias, Renee S. (Ed.)
    ABSTRACT

    Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.

    IMPORTANCE

    In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.

     
    more » « less
  2. Abstract

    Foliar fungal endophytes are ubiquitous plant symbionts that can affect plant growth and reproduction via their roles in pathogen and stress tolerance, as well as plant hormonal signaling. Despite their importance, we have a limited understanding of how foliar fungal endophytes respond to varying environmental conditions such as nutrient inputs. The responses of foliar fungal endophyte communities to increased nutrient deposition may be mediated by the simultaneous effects on within‐host competition as well as the indirect impacts of altered host population size, plant productivity, and plant community diversity and composition. Here, we leveraged a 7‐yr experiment manipulating nitrogen, phosphorus, potassium, and micronutrients to investigate how nutrient‐induced changes to plant diversity, plant productivity, and plant community composition relate to changes in foliar fungal endophyte diversity and richness in a focal native grass host,Andropogon gerardii. We found limited evidence of direct effects of nutrients on endophyte diversity. Instead, the effects of nutrients on endophyte diversity appeared to be mediated by accumulation of plant litter and plant diversity loss. Specifically, nitrogen addition is associated with a 40% decrease in plant diversity and an 11% decrease in endophyte richness. Although nitrogen, phosphorus, and potassium addition increased aboveground live biomass and decreased relativeAndropogoncover, endophyte diversity did not covary with live plant biomass orAndropogoncover. Our results suggest that fungal endophyte diversity within this focal host is determined in part by the diversity of the surrounding plant community and its potential impact on immigrant propagules and dispersal dynamics. Our results suggest that elemental nutrients reduce endophyte diversity indirectly via impacts on the local plant community, not direct response to nutrient addition. Thus, the effects of global change drivers, such as nutrient deposition, on characteristics of host populations and the diversity of their local communities are important for predicting the response of symbiont communities in a changing global environment.

     
    more » « less
  3. Abstract

    Intraspecific diversity of dominant species in native plant communities can modulate ecosystem function under both optimal and stressful conditions. Yet, few genotype by environment interaction studies quantify differences in the shape of plasticity functions or phenotypic breakpoints across genotypes in natural populations.

    Using three genotypes with a history of drought selection, we performed a greenhouse study on the dominant tallgrass prairie speciesAndropogon gerardii. We investigated phenotypic plasticity and recovery differences among genotypes across a water availability gradient, measuring growth‐related, instantaneous and cumulative phenotypes. To further understand genotype by environment effects, we quantified plasticity functions and breakpoints among genotypes.

    Like other studies, we found strong evidence for phenotypic and plasticity differences among genotypes. However, we also found nonlinear plasticity functions and breakpoints were common across phenotypes, especially relative growth rates, biomass allocation and root architecture. Drought selected genotypes were also more likely to flower during recovery, but all genotypes were resilient to drought across treatments.

    We demonstrate that plasticity functions may help explain intraspecific diversity, patterns of selection and nonlinear community responses to more variable rainfall within an experimental population. In particular, plasticity functions can help disentangle drought/variability tolerance versus acquisitive strategies. A better understanding of intraspecific diversity in this grass species will provide more mechanistic insight into its ability to buffer ecosystem changes and provide resiliency in the tallgrass prairie under future droughts.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  4. Abstract

    Grasslands of the central United States are expected to experience severe droughts and other climate extremes in the future, yet we know little about how these grasses will respond in terms of gene expression. We compared gene expression inAndropogon gerardiiandSorghastrum nutans, two closely related codominant C4grasses responsible for the majority of ecosystem function, usingRNA‐seq. We compared Trinity assemblies within each species to determine annotated functions of transcripts responding to drought. Subsequently, we compared homologous annotated gene‐groups across the two species using cross‐species meta‐level analysis and functional clustering based on key terms. The majority of variation was found between species, as opposed to between drought and watered treatments. However, there is evidence for differential responses;Andropogonallocated gene expression differently compared toSorghastrum, suggestingAndropogonfocuses on stress alleviation (such as oxygen radical scavenging) rather than prevention. In contrast,Sorghastrummay employ a drought avoidance strategy by modulating osmotic response, especially with hormonal regulation. We foundSorghastrumtended to be more sensitive within 10 key gene‐groups related to stress, abscisic acid and trichomes, suggesting gene expression may mechanistically parallel sensitivity at the physiological level. Our findings corroborate phenotypic and physiological differences in the field and may help explain the phenotypic mechanisms of these two species in the tallgrass prairie community under future drought scenarios.

     
    more » « less
  5. Summary

    As climate changes, many regions of the world are projected to experience more intense droughts, which can drive changes in plant community composition through a variety of mechanisms. During drought, community composition can respond directly to resource limitation, but biotic interactions modify the availability of these resources. Here, we develop the Community Response to Extreme Drought framework (CRED), which organizes the temporal progression of mechanisms and plant–plant interactions that may lead to community changes during and after a drought. TheCREDframework applies some principles of the stress gradient hypothesis (SGH), which proposes that the balance between competition and facilitation changes with increasing stress. TheCREDframework suggests that net biotic interactions (NBI), the relative frequency and intensity of facilitative (+) and competitive (−) interactions between plants, will change temporally, becoming more positive under increasing drought stress and more negative as drought stress decreases. Furthermore, we suggest that rewetting rates affect the rate of resource amelioration, specifically water and nitrogen, altering productivity responses and the intensity and importance ofNBI, all of which will influence drought‐induced compositional changes. System‐specific variables and the intensity of drought influence the strength of these interactions, and ultimately the system's resistance and resilience to drought.

     
    more » « less