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 gr...

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Autores principales: Shengjing Shi, Erin Nuccio, Donald J. Herman, Ruud Rijkers, Katerina Estera, Jiabao Li, Ulisses Nunes da Rocha, Zhili He, Jennifer Pett-Ridge, Eoin L. Brodie, Jizhong Zhou, Mary Firestone
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Publicado: American Society for Microbiology 2015
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spelling oai:doaj.org-article:35a74ab0d81e4dadbc2fb52da0410e7b2021-11-15T15:41:26ZSuccessional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons10.1128/mBio.00746-152150-7511https://doaj.org/article/35a74ab0d81e4dadbc2fb52da0410e7b2015-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00746-15https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE 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.Shengjing ShiErin NuccioDonald J. HermanRuud RijkersKaterina EsteraJiabao LiUlisses Nunes da RochaZhili HeJennifer Pett-RidgeEoin L. BrodieJizhong ZhouMary FirestoneAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 4 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Shengjing Shi
Erin Nuccio
Donald J. Herman
Ruud Rijkers
Katerina Estera
Jiabao Li
Ulisses Nunes da Rocha
Zhili He
Jennifer Pett-Ridge
Eoin L. Brodie
Jizhong Zhou
Mary Firestone
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
description 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 of its presence. IMPORTANCE 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.
format article
author Shengjing Shi
Erin Nuccio
Donald J. Herman
Ruud Rijkers
Katerina Estera
Jiabao Li
Ulisses Nunes da Rocha
Zhili He
Jennifer Pett-Ridge
Eoin L. Brodie
Jizhong Zhou
Mary Firestone
author_facet Shengjing Shi
Erin Nuccio
Donald J. Herman
Ruud Rijkers
Katerina Estera
Jiabao Li
Ulisses Nunes da Rocha
Zhili He
Jennifer Pett-Ridge
Eoin L. Brodie
Jizhong Zhou
Mary Firestone
author_sort Shengjing Shi
title Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
title_short Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
title_full Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
title_fullStr Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
title_full_unstemmed Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons
title_sort successional trajectories of rhizosphere bacterial communities over consecutive seasons
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/35a74ab0d81e4dadbc2fb52da0410e7b
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