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Title: Successional trajectories of rhizosphere bacterial communities over consecutive seasons

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 grass Avena fatua over 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 of Alphaproteobacteria, Betaproteobacteria, and Bacteroidetes but reduced the abundance of Acidobacteria, Actinobacteria, and Firmicutes. 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 ofmore » its presence. We 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 to Avena 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.« 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 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) (SC-23)
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. 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, and Firestone, Mary. Tue . "Successional trajectories of rhizosphere bacterial communities over consecutive seasons". United States. doi: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 = {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 grass Avena fatua over 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 of Alphaproteobacteria, Betaproteobacteria, and Bacteroidetes but reduced the abundance of Acidobacteria, Actinobacteria, and Firmicutes. 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. We 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 to Avena 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.},
doi = {10.1128/mBio.00746-15},
journal = {mBio (Online)},
number = 4,
volume = 6,
place = {United States},
year = {2015},
month = {8}
}

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