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Title: Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly

Abstract

Like all higher organisms, plants have evolved in the context of a microbial world, shaping both their evolution and their contemporary ecology. Interactions between plant roots and soil microorganisms are critical for plant fitness in natural environments. Given this co-evolution and the pivotal importance of plant–microbial interactions, it has been hypothesized, and a growing body of literature suggests, that plants may regulate the composition of their rhizosphere to promote the growth of microorganisms that improve plant fitness in a given ecosystem. In this paper, using a combination of comparative genomics and exometabolomics, we show that pre-programmed developmental processes in plants (Avena barbata) result in consistent patterns in the chemical composition of root exudates. This chemical succession in the rhizosphere interacts with microbial metabolite substrate preferences that are predictable from genome sequences. Specifically, we observed a preference by rhizosphere bacteria for consumption of aromatic organic acids exuded by plants (nicotinic, shikimic, salicylic, cinnamic and indole-3-acetic). The combination of these plant exudation traits and microbial substrate uptake traits interact to yield the patterns of microbial community assembly observed in the rhizosphere of an annual grass. Finally, this discovery provides a mechanistic underpinning for the process of rhizosphere microbial community assembly and providesmore » an attractive direction for the manipulation of the rhizosphere microbiome for beneficial outcomes.« less

Authors:
 [1];  [2]; ORCiD logo [3];  [4];  [5];  [6];  [7]; ORCiD logo [3];  [8];  [2];  [9]; ORCiD logo [2]; ORCiD logo [9]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division. Earth and Environmental Sciences
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division. Joint BioEnergy Inst. Biosystems Engineering Division
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences; Helmholtz Centre for Environmental Research - UFZ, Leipzig (Germany). Dept. of Environmental Microbiology
  6. AgResearch Ltd, Christchurch (New Zealand). Lincoln Science Centre
  7. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  8. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division. Joint BioEnergy Inst. Biosystems Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Claude Bernard Univ. Lyon 1, Villeurbanne (France). Microbiology, Adaptation and Pathogenesis
  9. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); European Union (EU); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division
OSTI Identifier:
1471041
Alternate Identifier(s):
OSTI ID: 1597099
Grant/Contract Number:  
AC02-05CH11231; SC0010570; SC0016247; SC0014079; 659910
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 4; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES

Citation Formats

Zhalnina, Kateryna, Louie, Katherine B., Hao, Zhao, Mansoori, Nasim, da Rocha, Ulisses Nunes, Shi, Shengjing, Cho, Heejung, Karaoz, Ulas, Loqué, Dominique, Bowen, Benjamin P., Firestone, Mary K., Northen, Trent R., and Brodie, Eoin L. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. United States: N. p., 2018. Web. doi:10.1038/s41564-018-0129-3.
Zhalnina, Kateryna, Louie, Katherine B., Hao, Zhao, Mansoori, Nasim, da Rocha, Ulisses Nunes, Shi, Shengjing, Cho, Heejung, Karaoz, Ulas, Loqué, Dominique, Bowen, Benjamin P., Firestone, Mary K., Northen, Trent R., & Brodie, Eoin L. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. United States. doi:10.1038/s41564-018-0129-3.
Zhalnina, Kateryna, Louie, Katherine B., Hao, Zhao, Mansoori, Nasim, da Rocha, Ulisses Nunes, Shi, Shengjing, Cho, Heejung, Karaoz, Ulas, Loqué, Dominique, Bowen, Benjamin P., Firestone, Mary K., Northen, Trent R., and Brodie, Eoin L. Mon . "Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly". United States. doi:10.1038/s41564-018-0129-3. https://www.osti.gov/servlets/purl/1471041.
@article{osti_1471041,
title = {Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly},
author = {Zhalnina, Kateryna and Louie, Katherine B. and Hao, Zhao and Mansoori, Nasim and da Rocha, Ulisses Nunes and Shi, Shengjing and Cho, Heejung and Karaoz, Ulas and Loqué, Dominique and Bowen, Benjamin P. and Firestone, Mary K. and Northen, Trent R. and Brodie, Eoin L.},
abstractNote = {Like all higher organisms, plants have evolved in the context of a microbial world, shaping both their evolution and their contemporary ecology. Interactions between plant roots and soil microorganisms are critical for plant fitness in natural environments. Given this co-evolution and the pivotal importance of plant–microbial interactions, it has been hypothesized, and a growing body of literature suggests, that plants may regulate the composition of their rhizosphere to promote the growth of microorganisms that improve plant fitness in a given ecosystem. In this paper, using a combination of comparative genomics and exometabolomics, we show that pre-programmed developmental processes in plants (Avena barbata) result in consistent patterns in the chemical composition of root exudates. This chemical succession in the rhizosphere interacts with microbial metabolite substrate preferences that are predictable from genome sequences. Specifically, we observed a preference by rhizosphere bacteria for consumption of aromatic organic acids exuded by plants (nicotinic, shikimic, salicylic, cinnamic and indole-3-acetic). The combination of these plant exudation traits and microbial substrate uptake traits interact to yield the patterns of microbial community assembly observed in the rhizosphere of an annual grass. Finally, this discovery provides a mechanistic underpinning for the process of rhizosphere microbial community assembly and provides an attractive direction for the manipulation of the rhizosphere microbiome for beneficial outcomes.},
doi = {10.1038/s41564-018-0129-3},
journal = {Nature Microbiology},
number = 4,
volume = 3,
place = {United States},
year = {2018},
month = {3}
}

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