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Title: Successional trajectories of rhizosphere bacterial communities over consecutive seasons

Abstract

ABSTRACT 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 grassAvena fatuaover 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 ofAlphaproteobacteria,Betaproteobacteria, andBacteroidetesbut reduced the abundance ofAcidobacteria,Actinobacteria, andFirmicutes. 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. IMPORTANCEWe document the successional patterns ofmore » 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 toAvenaroots. 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.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [6];  [5];  [7];  [3];  [8];  [3]
  1. Univ. of California, Berkeley, CA (United States); Univ. of Oklahoma, Norman, OK (United States)
  2. Univ. of California, Berkeley, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  3. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Univ. of California, Berkeley, CA (United States)
  5. Univ. of Oklahoma, Norman, OK (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  8. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1215423
Alternate Identifier(s):
OSTI ID: 1324516; OSTI ID: 1512225
Report Number(s):
LLNL-JRNL-671995
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
AC02-05CH11231; SA-DOE-29318; SC0004730; SC0010570; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 4; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL AND ANALYTICAL CHEMISTRY; 54 ENVIRONMENTAL SCIENCES; 58 GEOSCIENCES

Citation Formats

Shi, Shengjing, Nuccio, Erin, Herman, Donald J., Rijkers, Ruud, Estera, Katerina, Li, Jiabao, da Rocha, Ulisses Nunes, He, Zhili, Pett-Ridge, Jennifer, Brodie, Eoin L., Zhou, Jizhong, and Firestone, Mary. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. United States: N. p., 2015. Web. doi:10.1128/mBio.00746-15.
Shi, Shengjing, Nuccio, Erin, Herman, Donald J., Rijkers, Ruud, Estera, Katerina, Li, Jiabao, da Rocha, Ulisses Nunes, He, Zhili, Pett-Ridge, Jennifer, Brodie, Eoin L., Zhou, Jizhong, & Firestone, Mary. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. United States. https://doi.org/10.1128/mBio.00746-15
Shi, Shengjing, Nuccio, Erin, Herman, Donald J., Rijkers, Ruud, Estera, Katerina, Li, Jiabao, da Rocha, Ulisses Nunes, He, Zhili, Pett-Ridge, Jennifer, Brodie, Eoin L., Zhou, Jizhong, and Firestone, Mary. Tue . "Successional trajectories of rhizosphere bacterial communities over consecutive seasons". United States. https://doi.org/10.1128/mBio.00746-15. https://www.osti.gov/servlets/purl/1215423.
@article{osti_1215423,
title = {Successional trajectories of rhizosphere bacterial communities over consecutive seasons},
author = {Shi, Shengjing and Nuccio, Erin and Herman, Donald J. and Rijkers, Ruud and Estera, Katerina and Li, Jiabao and da Rocha, Ulisses Nunes and He, Zhili and Pett-Ridge, Jennifer and Brodie, Eoin L. and Zhou, Jizhong and Firestone, Mary},
abstractNote = {ABSTRACT 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 grassAvena fatuaover 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 ofAlphaproteobacteria,Betaproteobacteria, andBacteroidetesbut reduced the abundance ofAcidobacteria,Actinobacteria, andFirmicutes. 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. IMPORTANCEWe 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 toAvenaroots. 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.},
doi = {10.1128/mBio.00746-15},
journal = {mBio (Online)},
number = 4,
volume = 6,
place = {United States},
year = {Tue Aug 04 00:00:00 EDT 2015},
month = {Tue Aug 04 00:00:00 EDT 2015}
}

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Works referenced in this record:

Bulk and Rhizosphere Soil Bacterial Communities Studied by Denaturing Gradient Gel Electrophoresis: Plant-Dependent Enrichment and Seasonal Shifts Revealed
journal, October 2001


UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


A new method for non-parametric multivariate analysis of variance
journal, February 2001


In situ sampling of low molecular weight organic anions from rhizosphere of radiata pine (Pinus radiata) grown in a rhizotron system
journal, February 2011


Altered soil microbial community at elevated CO2 leads to loss of soil carbon
journal, March 2007

  • Carney, K. M.; Hungate, B. A.; Drake, B. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
  • DOI: 10.1073/pnas.0610045104

Coexistence of the Niche and Neutral Perspectives in Community Ecology
journal, June 2006


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

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


A new method for non-parametric multivariate analysis of variance
journal, February 2001


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

Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria
journal, May 2011


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009

  • Lauber, C. L.; Hamady, M.; Knight, R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 15
  • DOI: 10.1128/AEM.00335-09

Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups
journal, June 2012

  • Placella, S. A.; Brodie, E. L.; Firestone, M. K.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1204306109

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

The ecological coherence of high bacterial taxonomic ranks
journal, June 2010

  • Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J.
  • Nature Reviews Microbiology, Vol. 8, Issue 7
  • DOI: 10.1038/nrmicro2367

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


Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions
journal, February 2013


The generation and maintenance of diversity in microbial communities
journal, March 2011

  • Fierer, Noah; Lennon, Jay T.
  • American Journal of Botany, Vol. 98, Issue 3
  • DOI: 10.3732/ajb.1000498

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

Phylogenies and Community Ecology
journal, November 2002


Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA
journal, October 2007

  • Vandenkoornhuyse, P.; Mahe, S.; Ineson, P.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 43
  • DOI: 10.1073/pnas.0705902104

Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil
journal, April 2010


Mapping the niche space of soil microorganisms using taxonomy and traits
journal, August 2012

  • Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K.
  • Ecology, Vol. 93, Issue 8
  • DOI: 10.1890/11-1745.1

Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce
journal, April 2014


FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Rhizosphere microbiome assemblage is affected by plant development
journal, November 2013

  • Chaparro, Jacqueline M.; Badri, Dayakar V.; Vivanco, Jorge M.
  • The ISME Journal, Vol. 8, Issue 4
  • DOI: 10.1038/ismej.2013.196

Investigation of organic anions in tree root exudates and rhizosphere microbial communities using in situ and destructive sampling techniques
journal, March 2012

  • Shi, Shengjing; O’Callaghan, Maureen; Jones, E. Eirian
  • Plant and Soil, Vol. 359, Issue 1-2
  • DOI: 10.1007/s11104-012-1198-3

Effects of selected root exudate components on soil bacterial communities: Root exudate components and soil microbial communities
journal, July 2011


Exploration of hitherto-uncultured bacteria from the rhizosphere: Exploration of hitherto-unculturable bacteria
journal, September 2009


Phylogenetic diversity of Acidobacteria in a former agricultural soil
journal, November 2008

  • Kielak, Anna; Pijl, Agata S.; van Veen, Johannes A.
  • The ISME Journal, Vol. 3, Issue 3
  • DOI: 10.1038/ismej.2008.113

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Multivariate dispersion as a measure of beta diversity
journal, June 2006


Distance-Based Tests for Homogeneity of Multivariate Dispersions
journal, October 2005


Cross-biome metagenomic analyses of soil microbial communities and their functional attributes
journal, December 2012

  • Fierer, N.; Leff, J. W.; Adams, B. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
  • DOI: 10.1073/pnas.1215210110

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

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


Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar
journal, January 2014


Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays
journal, July 2005


Rhizosphere: biophysics, biogeochemistry and ecological relevance
journal, January 2009

  • Hinsinger, Philippe; Bengough, A. Glyn; Vetterlein, Doris
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-008-9885-9

Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance
journal, January 2011

  • Goldfarb, Katherine C.; Karaoz, Ulas; Hanson, China A.
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00094

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

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

APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms
journal, September 2013

  • Mendes, Rodrigo; Garbeva, Paolina; Raaijmakers, Jos M.
  • FEMS Microbiology Reviews, Vol. 37, Issue 5
  • DOI: 10.1111/1574-6976.12028

Prokaryotic Diversity--Magnitude, Dynamics, and Controlling Factors
journal, May 2002


Picante: R tools for integrating phylogenies and ecology
journal, April 2010


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

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


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

Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake
journal, March 2020


Defining the core Arabidopsis thaliana root microbiome
text, January 2012

  • E., Ley, Ruth; Julien, Tremblay,; L., Dangl, Jeffery
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/w03e-5q36

Diversity and heritability of the maize rhizosphere microbiome under field conditions
text, January 2013

  • Z., Jin,; S., Buckler, E.; O., Koren,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/rzga-0c56

Works referencing / citing this record:

Conservation tillage enhances the stability of the rhizosphere bacterial community responding to plant growth
journal, September 2017


Sugars altered fungal community composition and caused high network complexity in a Fusarium wilt pathogen-infested soil
journal, January 2020


Temperature drives the assembly of endophytic communities' seasonal succession
journal, July 2017

  • Campisano, Andrea; Albanese, Davide; Yousaf, Sohail
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13843

Plant growth and oil contamination alter the diversity and composition of bacterial communities in agricultural soils across China
journal, May 2018

  • Jiao, Shuo; Chen, Weimin; Wang, Junman
  • Land Degradation & Development, Vol. 29, Issue 6
  • DOI: 10.1002/ldr.2932

Plant Phylogeny and Life History Shape Rhizosphere Bacterial Microbiome of Summer Annuals in an Agricultural Field
journal, December 2017

  • Emmett, Bryan D.; Youngblut, Nicholas D.; Buckley, Daniel H.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02414

Understanding the phyllosphere microbiome assemblage in grape species (Vitaceae) with amplicon sequence data structures
journal, October 2019


Below-ground connections underlying above-ground food production: a framework for optimising ecological connections in the rhizosphere
journal, June 2017

  • de Vries, Franciska T.; Wallenstein, Matthew D.
  • Journal of Ecology, Vol. 105, Issue 4
  • DOI: 10.1111/1365-2745.12783

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

The aeroponic rhizosphere microbiome: community dynamics in early succession suggest strong selectional forces
journal, September 2019

  • Edmonds, Jennifer W.; Sackett, Joshua D.; Lomprey, Hunter
  • Antonie van Leeuwenhoek, Vol. 113, Issue 1
  • DOI: 10.1007/s10482-019-01319-y

Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis
journal, March 2019

  • Sheflin, Amy M.; Chiniquy, Dawn; Yuan, Chaohui
  • Plant Direct, Vol. 3, Issue 3
  • DOI: 10.1002/pld3.122

Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development
journal, December 2016

  • Pfeiffer, Stefan; Mitter, Birgit; Oswald, Andreas
  • FEMS Microbiology Ecology, Vol. 93, Issue 2
  • DOI: 10.1093/femsec/fiw242

Microbial community assembly differs across minerals in a rhizosphere microcosm
journal, September 2018

  • Whitman, Thea; Neurath, Rachel; Perera, Adele
  • Environmental Microbiology, Vol. 20, Issue 12
  • DOI: 10.1111/1462-2920.14366

Cadmium Exposure- Sedum alfredii Planting Interactions Shape the Bacterial Community in the Hyperaccumulator Plant Rhizosphere
journal, April 2018

  • Hou, Dandi; Lin, Zhi; Wang, Runze
  • Applied and Environmental Microbiology, Vol. 84, Issue 12
  • DOI: 10.1128/aem.02797-17

Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass
journal, May 2016

  • Nuccio, Erin E.; Anderson-Furgeson, James; Estera, Katerina Y.
  • Ecology, Vol. 97, Issue 5
  • DOI: 10.1890/15-0882.1

Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field
journal, October 2019

  • Emmett, Bryan D.; Buckley, Daniel H.; Drinkwater, Laurie E.
  • New Phytologist, Vol. 225, Issue 2
  • DOI: 10.1111/nph.16171

Soil abiotic variables are more important than Salicaceae phylogeny or habitat specialization in determining soil microbial community structure
journal, April 2018

  • Erlandson, Sonya; Wei, Xiaojing; Savage, Jessica
  • Molecular Ecology, Vol. 27, Issue 8
  • DOI: 10.1111/mec.14576

Belowground microbial communities respond to water deficit and are shaped by decades of maize hybrid breeding
journal, June 2019

  • Wang, Peng; Marsh, Ellen L.; Kruger, Greg
  • Environmental Microbiology, Vol. 22, Issue 3
  • DOI: 10.1111/1462-2920.14701

Impact of Cropping Systems, Soil Inoculum, and Plant Species Identity on Soil Bacterial Community Structure
journal, September 2016


Nutrient and Rainfall Additions Shift Phylogenetically Estimated Traits of Soil Microbial Communities
journal, July 2017


Microbial distribution and turnover in Antarctic microbial mats highlight the relevance of heterotrophic bacteria in low-nutrient environments
journal, June 2018

  • Valdespino-Castillo, Patricia M.; Cerqueda-García, Daniel; Espinosa, Ana Cecilia
  • FEMS Microbiology Ecology, Vol. 94, Issue 9
  • DOI: 10.1093/femsec/fiy129

Leaf endophytic fungus interacts with precipitation to alter belowground microbial communities in primary successional dunes
journal, March 2017

  • Bell-Dereske, Lukas; Takacs-Vesbach, Cristina; Kivlin, Stephanie N.
  • FEMS Microbiology Ecology, Vol. 93, Issue 6
  • DOI: 10.1093/femsec/fix036

Niche differentiation is spatially and temporally regulated in the rhizosphere
journal, January 2020