Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
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 im...
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| Published in | Nature microbiology Vol. 3; no. 4; pp. 470 - 480 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.04.2018
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| 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. Here, 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. 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.
Using comparative genomics and exometabolomics, the authors characterize the chemical composition of plant root exudates and show that this chemical succession is a likely driver of microbial community assembly in the rhizosphere. |
|---|---|
| AbstractList | 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. Here, 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. 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.
Using comparative genomics and exometabolomics, the authors characterize the chemical composition of plant root exudates and show that this chemical succession is a likely driver of microbial community assembly in the rhizosphere. 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. Here, 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. 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 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. Here, 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. 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. 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. Here, 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. 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.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. Here, 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. 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. 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. |
| Author | Hao, Zhao Loqué, Dominique Firestone, Mary K. Cho, Heejung Louie, Katherine B. Northen, Trent R. Bowen, Benjamin P. Brodie, Eoin L. Shi, Shengjing da Rocha, Ulisses Nunes Zhalnina, Kateryna Karaoz, Ulas Mansoori, Nasim |
| Author_xml | – sequence: 1 givenname: Kateryna surname: Zhalnina fullname: Zhalnina, Kateryna organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory – sequence: 2 givenname: Katherine B. surname: Louie fullname: Louie, Katherine B. organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory – sequence: 3 givenname: Zhao orcidid: 0000-0003-0677-8529 surname: Hao fullname: Hao, Zhao organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory – sequence: 4 givenname: Nasim surname: Mansoori fullname: Mansoori, Nasim organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Joint BioEnergy Institute, Biosystems Engineering Division, Lawrence Berkeley National Laboratory – sequence: 5 givenname: Ulisses Nunes surname: da Rocha fullname: da Rocha, Ulisses Nunes organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Department of Environmental Microbiology, Helmholtz Centre for Environmental Research—UFZ – sequence: 6 givenname: Shengjing surname: Shi fullname: Shi, Shengjing organization: Lincoln Science Centre, AgResearch Ltd – sequence: 7 givenname: Heejung surname: Cho fullname: Cho, Heejung organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Department of Plant and Microbial Biology, University of California – sequence: 8 givenname: Ulas orcidid: 0000-0002-8238-6757 surname: Karaoz fullname: Karaoz, Ulas organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory – sequence: 9 givenname: Dominique surname: Loqué fullname: Loqué, Dominique organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Joint BioEnergy Institute, Biosystems Engineering Division, Lawrence Berkeley National Laboratory, Department of Plant and Microbial Biology, University of California, INSA de Lyon, CNRS, UMR5240, Microbiologie, Adaptation et Pathogénie, Université Claude Bernard Lyon 1 – sequence: 10 givenname: Benjamin P. surname: Bowen fullname: Bowen, Benjamin P. organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory – sequence: 11 givenname: Mary K. surname: Firestone fullname: Firestone, Mary K. organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Department of Environmental Science, Policy and Management, University of California – sequence: 12 givenname: Trent R. orcidid: 0000-0001-8404-3259 surname: Northen fullname: Northen, Trent R. email: trnorthen@lbl.gov organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory – sequence: 13 givenname: Eoin L. orcidid: 0000-0002-8453-8435 surname: Brodie fullname: Brodie, Eoin L. email: elbrodie@lbl.gov organization: Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Department of Environmental Science, Policy and Management, University of California |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29556109$$D View this record in MEDLINE/PubMed https://hal.science/hal-02000374$$DView record in HAL https://www.osti.gov/servlets/purl/1471041$$D View this record in Osti.gov |
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| SubjectTerms | 45 45/22 45/23 45/77 631/326/171 631/326/2565 631/326/2565/855 631/449/2676/2678 631/92/320 Actinobacteria - isolation & purification Actinobacteria - metabolism Avena - metabolism Avena - microbiology BASIC BIOLOGICAL SCIENCES Biomedical and Life Sciences Cinnamates - metabolism ENVIRONMENTAL SCIENCES Exudates Firmicutes - isolation & purification Firmicutes - metabolism Genomics Host Microbial Interactions - physiology Indoleacetic Acids - metabolism Indoles Infectious Diseases Life Sciences Medical Microbiology Microbiology Microbiology and Parasitology Microbiomes Microbiota - physiology Microorganisms Niacin - metabolism Organic acids Parasitology Plant Roots - metabolism Plant Roots - microbiology Proteobacteria - isolation & purification Proteobacteria - metabolism Reproductive fitness Rhizosphere Rhizosphere microorganisms Salicylic Acid - metabolism Shikimic Acid - metabolism Soil Microbiology Soil microorganisms Substrate preferences Virology |
| Title | Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly |
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