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Title: Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots

Abstract

Abstract For a deeper and comprehensive understanding of the composition and function of rhizosphere microbiomes, we need to focus at the scale of individual roots in standardized growth containers. Root exudation patterns are known to vary along distinct parts of the root even in juvenile plants giving rise to spatially distinct microbial niches. To address this, we analyzed the microbial community from two spatially distinct zones of the developing primary root (tip and base) in young Brachypodium distachyon grown in natural soil using standardized fabricated ecosystems known as EcoFABs as well as in more conventional pot and tubes. 16S rRNA based community analysis showed a strong rhizosphere effect resulting in significant enrichment of several OTUs belonging to Actinobacteria, Bacteroidetes, Firmicutes and Proteobacteria. However, microbial community composition did not differ between root tips and root base or across different growth containers. Functional analysis of bulk metagenomics revealed significant differences between root tips and bulk soil. The genes associated with different metabolic pathways and root colonization were enriched in root tips. On the other hand, genes associated with nutrient-limitation and environmental stress were prominent in the bulk soil compared to root tips, implying the absence of easily available, labile carbon and nutrientsmore » in bulk soil relative to roots. Such insights into the relationships between developing root and microbial communities are critical for judicious understanding of plant-microbe interactions in early developmental stages of plants.« less

Authors:
; ; ORCiD logo; ; ; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1983999
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
ISME Communications
Additional Journal Information:
Journal Name: ISME Communications Journal Volume: 3 Journal Issue: 1; Journal ID: ISSN 2730-6151
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English

Citation Formats

Acharya, Shwetha M., Yee, Mon Oo, Diamond, Spencer, Andeer, Peter F., Baig, Nameera F., Aladesanmi, Omolara T., Northen, Trent R., Banfield, Jillian F., and Chakraborty, Romy. Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots. United States: N. p., 2023. Web. doi:10.1038/s43705-023-00265-1.
Acharya, Shwetha M., Yee, Mon Oo, Diamond, Spencer, Andeer, Peter F., Baig, Nameera F., Aladesanmi, Omolara T., Northen, Trent R., Banfield, Jillian F., & Chakraborty, Romy. Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots. United States. https://doi.org/10.1038/s43705-023-00265-1
Acharya, Shwetha M., Yee, Mon Oo, Diamond, Spencer, Andeer, Peter F., Baig, Nameera F., Aladesanmi, Omolara T., Northen, Trent R., Banfield, Jillian F., and Chakraborty, Romy. Tue . "Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots". United States. https://doi.org/10.1038/s43705-023-00265-1.
@article{osti_1983999,
title = {Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots},
author = {Acharya, Shwetha M. and Yee, Mon Oo and Diamond, Spencer and Andeer, Peter F. and Baig, Nameera F. and Aladesanmi, Omolara T. and Northen, Trent R. and Banfield, Jillian F. and Chakraborty, Romy},
abstractNote = {Abstract For a deeper and comprehensive understanding of the composition and function of rhizosphere microbiomes, we need to focus at the scale of individual roots in standardized growth containers. Root exudation patterns are known to vary along distinct parts of the root even in juvenile plants giving rise to spatially distinct microbial niches. To address this, we analyzed the microbial community from two spatially distinct zones of the developing primary root (tip and base) in young Brachypodium distachyon grown in natural soil using standardized fabricated ecosystems known as EcoFABs as well as in more conventional pot and tubes. 16S rRNA based community analysis showed a strong rhizosphere effect resulting in significant enrichment of several OTUs belonging to Actinobacteria, Bacteroidetes, Firmicutes and Proteobacteria. However, microbial community composition did not differ between root tips and root base or across different growth containers. Functional analysis of bulk metagenomics revealed significant differences between root tips and bulk soil. The genes associated with different metabolic pathways and root colonization were enriched in root tips. On the other hand, genes associated with nutrient-limitation and environmental stress were prominent in the bulk soil compared to root tips, implying the absence of easily available, labile carbon and nutrients in bulk soil relative to roots. Such insights into the relationships between developing root and microbial communities are critical for judicious understanding of plant-microbe interactions in early developmental stages of plants.},
doi = {10.1038/s43705-023-00265-1},
journal = {ISME Communications},
number = 1,
volume = 3,
place = {United States},
year = {Tue Jun 06 00:00:00 EDT 2023},
month = {Tue Jun 06 00:00:00 EDT 2023}
}

Works referenced in this record:

GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes
journal, March 2018

  • Boyd, Joel A.; Woodcroft, Ben J.; Tyson, Gene W.
  • Nucleic Acids Research, Vol. 46, Issue 10
  • DOI: 10.1093/nar/gky174

Carbon input by roots into the soil: Quantification of rhizodeposition from root to ecosystem scale
journal, September 2017

  • Pausch, Johanna; Kuzyakov, Yakov
  • Global Change Biology, Vol. 24, Issue 1
  • DOI: 10.1111/gcb.13850

Microbial community associated with ectomycorrhizal Russula symbiosis and dominated nature areas in southern China
journal, March 2021

  • Yu, Wen-Ying; Peng, Ming-Hui; Wang, Jia-Jia
  • FEMS Microbiology Letters, Vol. 368, Issue 6
  • DOI: 10.1093/femsle/fnab028

Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass
journal, January 2019

  • Sasse, Joelle; Kant, Josefine; Cole, Benjamin J.
  • New Phytologist, Vol. 222, Issue 2
  • DOI: 10.1111/nph.15662

Paenibacillus allorhizosphaerae sp. nov., from soil of the rhizosphere of Zea mays
journal, October 2021

  • Kämpfer, Peter; Busse, Hans-Jürgen; McInroy, John A.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 71, Issue 10
  • DOI: 10.1099/ijsem.0.005051

Spatial analysis of the root system coupled to microbial community inoculation shed light on rhizosphere bacterial community assembly
journal, August 2021

  • Wei, Shaodong; Jacquiod, Samuel; Philippot, Laurent
  • Biology and Fertility of Soils, Vol. 57, Issue 7
  • DOI: 10.1007/s00374-021-01590-0

SigB regulates stress resistance, glucose starvation, MnSOD production, biofilm formation, and root colonization in Bacillus cereus 905
journal, August 2021

  • Gao, Tantan; Li, Yan; Chai, Yunrong
  • Applied Microbiology and Biotechnology, Vol. 105, Issue 14-15
  • DOI: 10.1007/s00253-021-11402-y

Iron tolerance in rice: an efficient method for performing quick early genotype screening
journal, June 2019

  • Bresolin, Adriana Pires Soares; dos Santos, Railson Schreinert; Wolter, Roberto Carlos Doring
  • BMC Research Notes, Vol. 12, Issue 1
  • DOI: 10.1186/s13104-019-4362-5

Stimulation of Different Functional Groups of Bacteria by Various Plant Residues as a Driver of Soil Priming Effect
journal, February 2013


Specialized Plant Growth Chamber Designs to Study Complex Rhizosphere Interactions
journal, March 2021


Improved metagenome binning and assembly using deep variational autoencoders
journal, January 2021

  • Nissen, Jakob Nybo; Johansen, Joachim; Allesøe, Rosa Lundbye
  • Nature Biotechnology, Vol. 39, Issue 5
  • DOI: 10.1038/s41587-020-00777-4

Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation
journal, April 2021

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 49, Issue W1
  • DOI: 10.1093/nar/gkab301

EcoFABs: advancing microbiome science through standardized fabricated ecosystems
journal, June 2019


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Differential characterization of physiological and biochemical responses during drought stress in finger millet varieties
journal, May 2019

  • Mukami, Asunta; Ngetich, Alex; Mweu, Cecilia
  • Physiology and Molecular Biology of Plants, Vol. 25, Issue 4
  • DOI: 10.1007/s12298-019-00679-z

Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat
journal, October 2016


Effect of container type and seedling size on survival and early height growth of Pinus palustris seedlings in Alabama, U.S.A.
journal, January 2005


Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015


MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


Assembly Patterns of the Rhizosphere Microbiome Along the Longitudinal Root Axis of Maize (Zea mays L.)
journal, February 2021


Paenibacillus rhizophilus sp. nov., a nitrogen-fixing bacterium isolated from the rhizosphere of wheat (Triticum aestivum L.)
journal, December 2019

  • Ripa, Farhana Alam; Tong, Shuai; Cao, Wei-dong
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 12
  • DOI: 10.1099/ijsem.0.003472

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Actinobacterial community dominated by a distinct clade in acidic soil of a waterlogged deciduous forest
journal, August 2011


Genomic and phenotypic insights into the ecology of Arthrobacter from Antarctic soils
journal, February 2015


Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands
journal, October 2019


The structure and function of the global citrus rhizosphere microbiome
journal, November 2018


Metabolic responses of wheat seedlings to osmotic stress induced by various osmolytes under iso-osmotic conditions
journal, December 2019


Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy
journal, May 2018

  • Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison
  • Nature Microbiology, Vol. 3, Issue 7
  • DOI: 10.1038/s41564-018-0171-1

The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops
journal, January 2009

  • Watt, Michelle; Schneebeli, Katharina; Dong, Pan
  • Functional Plant Biology, Vol. 36, Issue 11
  • DOI: 10.1071/FP09214

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Error filtering, pair assembly and error correction for next-generation sequencing reads
journal, July 2015


Variation in genomic traits of microbial communities among ecosystems
journal, December 2021


GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database
journal, November 2019


Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

A Re-Examination of the Relative Turgidity Technique for Estimating Water Deficits in Leaves
journal, January 1962

  • Barrs, Hd; Weatherley, Pe
  • Australian Journal of Biological Sciences, Vol. 15, Issue 3
  • DOI: 10.1071/BI9620413

Root type is not an important driver of mycorrhizal colonisation in Brachypodium distachyon
journal, November 2017


Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum
journal, January 2002


Soil microbial community composition in tallgrass prairie restorations converge with remnants across a 27‐year chronosequence
journal, July 2017

  • Barber, Nicholas A.; Chantos‐Davidson, Karley M.; Amel Peralta, Rene
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13785

Evolution of bacterial communities in the wheat crop rhizosphere: Rhizosphere bacteria in field-grown intensive wheat crops
journal, May 2014

  • Donn, Suzanne; Kirkegaard, John A.; Perera, Geetha
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12452

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Effects of fertilization and container-type on nutrient uptake and utilization by four subtropical tree seedlings
journal, November 2019


dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication
journal, July 2017

  • Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.126

Ultra-accurate microbial amplicon sequencing with synthetic long reads
journal, June 2021


Nursery Practices Influence Seedling Morphology, Field Performance, and Cost Efficiency of Containerized Cherrybark Oak
journal, August 2004

  • Howell, Kirk D.; Harrington, Timothy B.
  • Southern Journal of Applied Forestry, Vol. 28, Issue 3
  • DOI: 10.1093/sjaf/28.3.152

Using DECIPHER v2.0 to Analyze Big Biological Sequence Data in R
journal, January 2016


KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold
journal, November 2019


Hotspots of root-exuded amino acids are created within a rhizosphere-on-a-chip
journal, January 2022

  • Aufrecht, Jayde; Khalid, Muneeba; Walton, Courtney L.
  • Lab on a Chip, Vol. 22, Issue 5
  • DOI: 10.1039/D1LC00705J

Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?: Root exudates and rhizosphere bacteria
journal, March 2010


Accelerated Growth Rate and Increased Drought Stress Resilience of the Model Grass Brachypodium distachyon Colonized by Bacillus subtilis B26
journal, June 2015


FtsEX-CwlO regulates biofilm formation by a plant-beneficial rhizobacterium Bacillus velezensis SQR9
journal, April 2018


ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences
journal, June 2017

  • Lee, Imchang; Chalita, Mauricio; Ha, Sung-Min
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 6
  • DOI: 10.1099/ijsem.0.001872

Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition
journal, April 2015

  • Tkacz, Andrzej; Cheema, Jitender; Chandra, Govind
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.41

The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016

  • Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
  • Ecology Letters, Vol. 19, Issue 8
  • DOI: 10.1111/ele.12630

Diazotroph Paenibacillus triticisoli BJ-18 Drives the Variation in Bacterial, Diazotrophic and Fungal Communities in the Rhizosphere and Root/Shoot Endosphere of Maize
journal, February 2021

  • Li, Yongbin; Li, Qin; Chen, Sanfeng
  • International Journal of Molecular Sciences, Vol. 22, Issue 3
  • DOI: 10.3390/ijms22031460

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013