skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.


Title: Zea mays genotype influences microbial and viral rhizobiome community structure
Abstract

Plant genotype is recognized to contribute to variations in microbial community structure in the rhizosphere, soil adherent to roots. However, the extent to which the viral community varies has remained poorly understood and has the potential to contribute to variation in soil microbial communities. Here we cultivated replicates of two Zea mays genotypes, parviglumis and B73, in a greenhouse and harvested the rhizobiome (rhizoplane and rhizosphere) to identify the abundance of cells and viruses as well as rhizobiome microbial and viral community using 16S rRNA gene amplicon sequencing and genome resolved metagenomics. Our results demonstrated that viruses exceeded microbial abundance in the rhizobiome of parviglumis and B73 with a significant variation in both the microbial and viral community between the two genotypes. Of the viral contigs identified only 4.5% (n = 7) of total viral contigs were shared between the two genotypes, demonstrating that plants even at the level of genotype can significantly alter the surrounding soil viral community. An auxiliary metabolic gene associated with glycoside hydrolase (GH5) degradation was identified in one viral metagenome-assembled genome (vOTU) identified in the B73 rhizobiome infecting Propionibacteriaceae (Actinobacteriota) further demonstrating the viral contribution in metabolic potential for carbohydrate degradation and carbon cycling in the rhizosphere. This variation demonstrates the potential of plant genotype to contribute to microbial and viral heterogeneity in soil systems and harbors genes capable of contributing to carbon cycling in the rhizosphere.

 
more » « less
NSF-PAR ID:
10478151
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
ISME Communications
Volume:
3
Issue:
1
ISSN:
2730-6151
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. The root-associated microbiome (rhizobiome) affects plant health, stress tolerance, and nutrient use efficiency. However, it remains unclear to what extent the composition of the rhizobiome is governed by intraspecific variation in host plant genetics in the field and the degree to which host plant selection can reshape the composition of the rhizobiome. Here, we quantify the rhizosphere microbial communities associated with a replicated diversity panel of 230 maize ( Zea mays L .) genotypes grown in agronomically relevant conditions under high N (+N) and low N (-N) treatments. We analyze the maize rhizobiome in terms of 150 abundant and consistently reproducible microbial groups and we show that the abundance of many root-associated microbes is explainable by natural genetic variation in the host plant, with a greater proportion of microbial variance attributable to plant genetic variation in -N conditions. Population genetic approaches identify signatures of purifying selection in the maize genome associated with the abundance of several groups of microbes in the maize rhizobiome. Genome-wide association study was conducted using the abundance of microbial groups as rhizobiome traits, and n=622 plant loci were identified that are linked to the abundance of n=104 microbial groups in the maize rhizosphere. In 62/104 cases, which is more than expected by chance, the abundance of these same microbial groups was correlated with variation in plant vigor indicators derived from high throughput phenotyping of the same field experiment. We provide comprehensive datasets about the three-way interaction of host genetics, microbe abundance, and plant performance under two N treatments to facilitate targeted experiments toward harnessing the full potential of root-associated microbial symbionts in maize production. 
    more » « less
  2. Abstract Background

    Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether viruses are active under winter conditions (anoxic and sub-freezing temperatures).

    Results

    We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under simulated winter conditions, with an emphasis on viruses and virus-host dynamics. Arctic peat soils from the Bonanza Creek Long-Term Ecological Research site in Alaska were incubated under sub-freezing anoxic conditions with H218O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO2) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up18O in soil and respired CO2throughout the incubation. Active bacterial populations represented only a small portion of the detected microbial community and were capable of fermentation and organic matter degradation. In contrast, active viral populations represented a large portion of the detected viral community and one third were linked to active bacterial populations. We identified 86 auxiliary metabolic genes and other environmentally relevant genes. The majority of these genes were carried by active viral populations and had diverse functions such as carbon utilization and scavenging that could provide their host with a fitness advantage for utilizing much-needed carbon sources or acquiring essential nutrients.

    Conclusions

    Overall, there was a stark difference in the identity and function of the active bacterial and viral community compared to the unlabeled community that would have been overlooked with a non-targeted standard metagenomic analysis. Our results illustrate that substantial active virus-host interactions occur in sub-freezing anoxic conditions and highlight viruses as a major community-structuring agent that likely modulates carbon loss in peat soils during winter, which may be pivotal for understanding the future fate of arctic soils' vast carbon stocks.

     
    more » « less
  3. 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
  4. Summary

    The ability of plant somatic cells to dedifferentiate, form somatic embryos and regenerate whole plantsin vitrohas been harnessed for both clonal propagation and as a key component of plant genetic engineering systems. Embryogenic culture response is significantly limited, however, by plant genotype in most species. This impedes advancements in both plant transformation‐based functional genomics research and crop improvement efforts. We utilized natural variation among maize inbred lines to genetically map somatic embryo generation potential in tissue culture and identify candidate genes underlying totipotency. Using a series of maize lines derived from crosses involving the culturable parent A188 and the non‐responsive parent B73, we identified a region on chromosome 3 associated with embryogenic culture response and focused on three candidate genes within the region based on genetic position and expression pattern. Two candidate genes showed no effect when ectopically expressed in B73, but the geneWox2awas found to induce somatic embryogenesis and embryogenic callus proliferation. Transgenic B73 cells with strong constitutive expression of the B73 and A188 coding sequences ofWox2awere found to produce somatic embryos at similar frequencies, demonstrating that sufficient expression of either allele could rescue the embryogenic culture phenotype. Transgenic B73 plants were regenerated from the somatic embryos without chemical selection and no pleiotropic effects were observed in theWox2aoverexpression lines in the regenerated T0 plants or in the two independent events which produced T1 progeny. In addition to linking natural variation in tissue culture response toWox2a, our data support the utility ofWox2ain enabling transformation of recalcitrant genotypes.

     
    more » « less
  5. Abstract

    The rhizosphere microbiome influences many aspects of plant fitness, including production of secondary compounds and defence against insect herbivores. Plants also modulate the composition of the microbial community in the rhizosphere via secretion of root exudates. We tested both the effect of the rhizosphere microbiome on plant traits, and host plant effects on rhizosphere microbes using recombinant inbred lines (RILs) ofBrassica rapathat differ in production of glucosinolates (GLS), secondary metabolites that contribute to defence against insect herbivores. First, we investigated the effect of genetic variation in GLS production on the composition of the rhizosphere microbiome. Using a Bayesian Dirichlet‐multinomial regression model (DMBVS), we identified both negative and positive associations between bacteria from six genera and the concentration of five GLS compounds produced in plant roots. Additionally, we tested the effects of microbial inoculation (an intact vs. disrupted soil microbiome) on GLS production and insect damage in these RILs. We found a significant microbial treatment × genotype interaction, in which total GLS was higher in the intact relative to the disrupted microbiome treatment in some RILs. However, despite differences in GLS production between microbial treatments, we observed no difference in insect damage between treatments. Together, these results provide evidence for a full feedback cycle of plant–microbe interactions mediated by GLS; that is, GLS compounds produced by the host plant “feed‐down” to influence rhizosphere microbial community and rhizosphere microbes “feed‐up” to influence GLS production.

     
    more » « less