skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass

Abstract

The interface between roots and soil, known as the rhizosphere, is a dynamic habitat in the soil ecosystem. Unraveling the factors that control rhizosphere community assembly is a key starting point for understanding the diversity of plant-microbial interactions that occur in soil. The goals of this study were to determine how environmental factors shape rhizosphere microbial communities, such as local soil characteristics and the regional climate, and to determine the relative influence of the rhizosphere on microbial community assembly compared to the pressures imposed by the local and regional environment. We identified the bacteria present in the soil immediately adjacent to the roots of wild oat (Avena spp.) in three California grasslands using deep Illumina 16S sequencing. Rhizosphere communities were more similar to each other than to the surrounding soil communities from which they were derived, despite the fact that the grasslands studied were separated by hundreds of kilometers. The rhizosphere was the dominant factor structuring bacterial community composition (38% variance explained), and was comparable in magnitude to the combined local and regional effects (22% and 21%, respectively). Rhizosphere communities were most influenced by factors related to the regional climate (soil moisture and temperature), while background soil communities were moremore » influenced by soil characteristics (pH, CEC, exchangeable cations, clay content). The Avena core microbiome was strongly phylogenetically clustered according to the metrics NRI and NTI, which indicates that selective processes likely shaped these communities. Furthermore, 17% of these taxa were not detectable in the background soil, even with a robust sequencing depth of approximately 70,000 sequences per sample. In conclusion, these results support the hypothesis that roots select less abundant or possibly rare populations in the soil microbial community, which appear to be lineages of bacteria that have made a physiological tradeoff for rhizosphere competence at the expense of their competitiveness in non-rhizosphere soil.« less

Authors:
 [1];  [2];  [3];  [4];  [3];  [5];  [5]
  1. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  2. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  3. Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
  5. Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management; Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Earth and Environmental Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1581117
Alternate Identifier(s):
OSTI ID: 1325886; OSTI ID: 1400974; OSTI ID: 1440928
Report Number(s):
LLNL-JRNL-670998
Journal ID: ISSN 0012-9658; ark:/13030/qt4rp9k2qg
Grant/Contract Number:  
AC02-05CH11231; AC52-07NA27344; SC0004730; SC0010570; SCW1421
Resource Type:
Accepted Manuscript
Journal Name:
Ecology
Additional Journal Information:
Journal Volume: 97; Journal Issue: 5; Journal ID: ISSN 0012-9658
Publisher:
Ecological Society of America (ESA)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; rhizosphere; microbiome; plant-microbial interactions; community assembly; soil; climate; Avena

Citation Formats

Nuccio, Erin E., Anderson-Furgeson, James, Estera, Katerina Y., Pett-Ridge, Jennifer, de Valpine, Perry, Brodie, Eoin L., and Firestone, Mary K. Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. United States: N. p., 2016. Web. doi:10.1890/15-0882.1.
Nuccio, Erin E., Anderson-Furgeson, James, Estera, Katerina Y., Pett-Ridge, Jennifer, de Valpine, Perry, Brodie, Eoin L., & Firestone, Mary K. Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. United States. doi:10.1890/15-0882.1.
Nuccio, Erin E., Anderson-Furgeson, James, Estera, Katerina Y., Pett-Ridge, Jennifer, de Valpine, Perry, Brodie, Eoin L., and Firestone, Mary K. Tue . "Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass". United States. doi:10.1890/15-0882.1. https://www.osti.gov/servlets/purl/1581117.
@article{osti_1581117,
title = {Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass},
author = {Nuccio, Erin E. and Anderson-Furgeson, James and Estera, Katerina Y. and Pett-Ridge, Jennifer and de Valpine, Perry and Brodie, Eoin L. and Firestone, Mary K.},
abstractNote = {The interface between roots and soil, known as the rhizosphere, is a dynamic habitat in the soil ecosystem. Unraveling the factors that control rhizosphere community assembly is a key starting point for understanding the diversity of plant-microbial interactions that occur in soil. The goals of this study were to determine how environmental factors shape rhizosphere microbial communities, such as local soil characteristics and the regional climate, and to determine the relative influence of the rhizosphere on microbial community assembly compared to the pressures imposed by the local and regional environment. We identified the bacteria present in the soil immediately adjacent to the roots of wild oat (Avena spp.) in three California grasslands using deep Illumina 16S sequencing. Rhizosphere communities were more similar to each other than to the surrounding soil communities from which they were derived, despite the fact that the grasslands studied were separated by hundreds of kilometers. The rhizosphere was the dominant factor structuring bacterial community composition (38% variance explained), and was comparable in magnitude to the combined local and regional effects (22% and 21%, respectively). Rhizosphere communities were most influenced by factors related to the regional climate (soil moisture and temperature), while background soil communities were more influenced by soil characteristics (pH, CEC, exchangeable cations, clay content). The Avena core microbiome was strongly phylogenetically clustered according to the metrics NRI and NTI, which indicates that selective processes likely shaped these communities. Furthermore, 17% of these taxa were not detectable in the background soil, even with a robust sequencing depth of approximately 70,000 sequences per sample. In conclusion, these results support the hypothesis that roots select less abundant or possibly rare populations in the soil microbial community, which appear to be lineages of bacteria that have made a physiological tradeoff for rhizosphere competence at the expense of their competitiveness in non-rhizosphere soil.},
doi = {10.1890/15-0882.1},
journal = {Ecology},
number = 5,
volume = 97,
place = {United States},
year = {2016},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006


Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

Quantitative imaging of rhizosphere pH and CO2 dynamics with planar optodes
journal, March 2013

  • Blossfeld, Stephan; Schreiber, Christina Maria; Liebsch, Gregor
  • Annals of Botany, Vol. 112, Issue 2
  • DOI: 10.1093/aob/mct047

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


Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley
journal, March 2015

  • Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C.
  • Cell Host & Microbe, Vol. 17, Issue 3
  • DOI: 10.1016/j.chom.2015.01.011

Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Patterns of Genetic Differentiation in the Slender Wild Oat Species Avena barbata
journal, July 1972

  • Clegg, M. T.; Allard, R. W.
  • Proceedings of the National Academy of Sciences, Vol. 69, Issue 7
  • DOI: 10.1073/pnas.69.7.1820

Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland
journal, March 2009

  • Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L.
  • The ISME Journal, Vol. 3, Issue 6
  • DOI: 10.1038/ismej.2009.16

Assembly of root-associated bacteria communities: interactions between abiotic and biotic factors: Plant-bacteria response to N pollution
journal, August 2014

  • Dean, Sarah L.; Farrer, Emily C.; Porras-Alfaro, Andrea
  • Environmental Microbiology Reports, Vol. 7, Issue 1
  • DOI: 10.1111/1758-2229.12194

Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

Bacterial quorum sensing and nitrogen cycling in rhizosphere soil: Bacterial QS and rhizosphere nitrogen cycling
journal, November 2008


Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis
journal, August 2004


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


Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review
journal, April 2011

  • Doornbos, Rogier F.; van Loon, Leendert Cornelis; Bakker, Peter A. H. M.
  • Agronomy for Sustainable Development, Vol. 32, Issue 1
  • DOI: 10.1007/s13593-011-0028-y

Electing a candidate: a speculative history of the bacterial phylum OP10: Discovery of OP10
journal, April 2012


Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015

  • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1414592112

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839

Distantly sampled soils carry few species in common
journal, June 2008

  • Fulthorpe, Roberta R.; Roesch, Luiz F. W.; Riva, Alberto
  • The ISME Journal, Vol. 2, Issue 9
  • DOI: 10.1038/ismej.2008.55

The Evolution of Ecological Specialization
journal, November 1988


Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.)
journal, May 1998


Finer resolution observation and monitoring of global land cover: first mapping results with Landsat TM and ETM+ data
journal, December 2012


Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition
journal, December 2000


Plant host habitat and root exudates shape soil bacterial community structure
journal, August 2008

  • Haichar, Feth el Zahar; Marol, Christine; Berge, Odile
  • The ISME Journal, Vol. 2, Issue 12
  • DOI: 10.1038/ismej.2008.80

Plant invasion alters nitrogen cycling by modifying the soil nitrifying community
journal, September 2005


Arbuscular Mycorrhizal Assemblages in Native Plant Roots Change in the Presence of Invasive Exotic Grasses
journal, March 2006


Root surface as a frontier for plant microbiome research: Fig. 1.
journal, February 2015

  • van der Heijden, Marcel G. A.; Schlaeppi, Klaus
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1500709112

Root Influence on Nitrogen Mineralization and Nitrification in Rhizosphere Soil
journal, January 2006

  • Herman, D. J.; Johnson, K. K.; Jaeger, C. H.
  • Soil Science Society of America Journal, Vol. 70, Issue 5
  • DOI: 10.2136/sssaj2005.0113

Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review
journal, January 2003

  • Hinsinger, Philippe; Plassard, Claude; Tang, Caixian
  • Plant and Soil, Vol. 248, Issue 1/2
  • DOI: 10.1023/A:1022371130939

Plant and soil nitrogen dynamics in California annual grassland
journal, August 1988

  • Jackson, L. E.; Strauss, R. B.; Firestone, M. K.
  • Plant and Soil, Vol. 110, Issue 1
  • DOI: 10.1007/BF02143533

A global analysis of root distributions for terrestrial biomes
journal, November 1996

  • Jackson, R. B.; Canadell, J.; Ehleringer, J. R.
  • Oecologia, Vol. 108, Issue 3
  • DOI: 10.1007/BF00333714

Rapid shifts in plant distribution with recent climate change
journal, August 2008

  • Kelly, A. E.; Goulden, M. L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
  • DOI: 10.1073/pnas.0802891105

Testing for local adaptation in Avena barbata : a classic example of ecotypic divergence
journal, September 2009


Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Root-induced changes in the rhizosphere: Importance for the mineral nutrition of plants
journal, January 1986

  • Marschner, H.; Römheld, V.; Horst, W. J.
  • Zeitschrift für Pflanzenernährung und Bodenkunde, Vol. 149, Issue 4
  • DOI: 10.1002/jpln.19861490408

Patterns and Processes of Microbial Community Assembly
journal, September 2013

  • Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
  • Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
  • DOI: 10.1128/MMBR.00051-12

Spatial Analysis of Archaeal Community Structure in Grassland Soil
journal, December 2003


Verrucomicrobia subdivision 1 strains display a difference in the colonization of the leek (Allium porrum) rhizosphere: Rhizosphere colonization by Verrucomicrobia strains
journal, July 2011


Selection on soil microbiomes reveals reproducible impacts on plant function
journal, October 2014

  • Panke-Buisse, Kevin; Poole, Angela C.; Goodrich, Julia K.
  • The ISME Journal, Vol. 9, Issue 4
  • DOI: 10.1038/ismej.2014.196

Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013

  • Peiffer, J. A.; Spor, A.; Koren, O.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
  • DOI: 10.1073/pnas.1302837110

Going back to the roots: the microbial ecology of the rhizosphere
journal, September 2013

  • Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3109

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


In Situ Phylogenetic Structure and Diversity of Wild Bradyrhizobium Communities
journal, May 2009

  • Sachs, J. L.; Kembel, S. W.; Lau, A. H.
  • Applied and Environmental Microbiology, Vol. 75, Issue 14
  • DOI: 10.1128/AEM.00667-09

Molecular evidence on plant divergence times
journal, October 2004

  • Sanderson, Michael J.; Thorne, Jeffrey L.; Wikström, Niklas
  • American Journal of Botany, Vol. 91, Issue 10
  • DOI: 10.3732/ajb.91.10.1656

Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives
journal, December 2013

  • Schlaeppi, K.; Dombrowski, N.; Oter, R. G.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
  • DOI: 10.1073/pnas.1321597111

Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
journal, August 2015


Stochastic and deterministic assembly processes in subsurface microbial communities
journal, March 2012

  • Stegen, James C.; Lin, Xueju; Konopka, Allan E.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.22

Quantifying community assembly processes and identifying features that impose them
journal, June 2013

  • Stegen, James C.; Lin, Xueju; Fredrickson, Jim K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.93

Plant growth-promoting rhizobacteria and root system functioning
journal, January 2013

  • Vacheron, Jordan; Desbrosses, Guilhem; Bouffaud, Marie-Lara
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00356

Emerging patterns in the comparative analysis of phylogenetic community structure
journal, February 2009


Conceptual Synthesis in Community Ecology
journal, June 2010

  • Vellend, Mark
  • The Quarterly Review of Biology, Vol. 85, Issue 2
  • DOI: 10.1086/652373

Soil biodiversity and soil community composition determine ecosystem multifunctionality
journal, March 2014

  • Wagg, C.; Bender, S. F.; Widmer, F.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
  • DOI: 10.1073/pnas.1320054111

Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes
journal, February 2013


Phylogenies and Community Ecology
journal, November 2002


Variation of Microbial Communities in Soil, Rhizosphere, and Rhizoplane in Response to Crop Species, Soil Type, and Crop Development
journal, December 2001


    Works referencing / citing this record:

    Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance
    journal, March 2019

    • Duhamel, Marie; Wan, Joe; Bogar, Laura M.
    • Ecological Monographs, Vol. 89, Issue 3
    • DOI: 10.1002/ecm.1367

    Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance
    journal, March 2019

    • Duhamel, Marie; Wan, Joe; Bogar, Laura M.
    • Ecological Monographs, Vol. 89, Issue 3
    • DOI: 10.1002/ecm.1367

    Microbiome Dynamics Associated With the Atacama Flowering Desert
    journal, January 2020

    • Araya, Juan Pablo; González, Máximo; Cardinale, Massimiliano
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.03160