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Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

Nameer R. Baker, Kateryna Zhalnina, Mengting Yuan, Don Herman, Javier A. Ceja-Navarro, Joelle Sasse, Jacob S. Jordan, Benjamin P. Bowen, Liyou Wu, Christina Fossum, Aaron Chew, Ying Fu, Malay Saha, Jizhong Zhou, Jennifer Pett-Ridge, Trent R. Northen, Mary Firestone
doi: https://doi.org/10.1101/2022.06.20.496911
Nameer R. Baker
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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Kateryna Zhalnina
bEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
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Mengting Yuan
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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Don Herman
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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Javier A. Ceja-Navarro
cBiological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
dInstitute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, California, USA
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Joelle Sasse
bEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
ePlant and Microbial Biology, University of Zurich, CH-8008 Zurich, Switzerland
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Jacob S. Jordan
bEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
fDepartment of Chemistry, University of California, Berkeley, CA 94720
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Benjamin P. Bowen
bEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
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Liyou Wu
gUniversity of Oklahoma, Norman, OK 73019
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Christina Fossum
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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Aaron Chew
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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Ying Fu
gUniversity of Oklahoma, Norman, OK 73019
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Malay Saha
hNoble Research Institute, Ardmore, OK 73401
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Jizhong Zhou
gUniversity of Oklahoma, Norman, OK 73019
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Jennifer Pett-Ridge
iPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA 94550
jLife and Environmental Sciences Department, University of California Merced, Merced, CA 95343
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Trent R. Northen
bEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
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Mary Firestone
aDepartment of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720
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  • For correspondence: mkfstone@berkeley.edu
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Abstract

Plants exude large quantities of rhizosphere metabolites that can modulate composition and activity of microbial communities in response to environmental stress. While rhizodeposition dynamics have been associated with rhizosphere microbiome succession, and may be particularly impactful in stressful conditions, specific evidence of these connections has rarely been documented. Here, we grew the bioenergy crop switchgrass (Panicum virgatum) in a marginal soil, under nutrient limited, moisture limited, +nitrogen (N), and +phosphorus (P) conditions, to identify links between rhizosphere chemistry, microbiome dynamics, and abiotic stressors. To characterize links between rhizosphere microbial communities and metabolites, we used 16S rRNA amplicon sequencing and LC-MS/MS-based metabolomics. We measured significant changes in rhizosphere metabolite profiles in response to abiotic stress and linked them to changes in microbial communities using network analysis. N-limitation amplified the abundance of aromatic acids, pentoses, and their derivatives in the rhizosphere, and their enhanced availability was linked to the abundance of diverse bacterial lineages from Acidobacteria, Verrucomicrobia, Planctomycetes, and Alphaproteobacteria. Conversely, N-amended conditions enhanced the availability of N-rich rhizosphere compounds, which coincided with proliferation of Actinobacteria. Treatments with contrasting N availability differed greatly in the abundance of potential keystone metabolites; serotonin, ectoine, and acetylcholine were particularly abundant in N-replete soils, while chlorogenic, cinnamic, and glucuronic acids were found in N-limited soils. Serotonin, the keystone metabolite we identified with the largest number of links to microbial taxa, significantly affected root architecture and growth of rhizosphere microorganisms, highlighting its potential to shape microbial community and mediate rhizosphere plant-microbe interactions.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 21, 2022.
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Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics
Nameer R. Baker, Kateryna Zhalnina, Mengting Yuan, Don Herman, Javier A. Ceja-Navarro, Joelle Sasse, Jacob S. Jordan, Benjamin P. Bowen, Liyou Wu, Christina Fossum, Aaron Chew, Ying Fu, Malay Saha, Jizhong Zhou, Jennifer Pett-Ridge, Trent R. Northen, Mary Firestone
bioRxiv 2022.06.20.496911; doi: https://doi.org/10.1101/2022.06.20.496911
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Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics
Nameer R. Baker, Kateryna Zhalnina, Mengting Yuan, Don Herman, Javier A. Ceja-Navarro, Joelle Sasse, Jacob S. Jordan, Benjamin P. Bowen, Liyou Wu, Christina Fossum, Aaron Chew, Ying Fu, Malay Saha, Jizhong Zhou, Jennifer Pett-Ridge, Trent R. Northen, Mary Firestone
bioRxiv 2022.06.20.496911; doi: https://doi.org/10.1101/2022.06.20.496911

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