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Research Article | Applied and Environmental Science

Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations

Taniya Roy Chowdhury, Joon-Yong Lee, Eric M. Bottos, Colin J. Brislawn, Richard Allen White III, Lisa M. Bramer, Joseph Brown, Jeremy D. Zucker, Young-Mo Kim, Ari Jumpponen, Charles W. Rice, Sarah J. Fansler, Thomas O. Metz, Lee Ann McCue, Stephen J. Callister, Hyun-Seob Song, Janet K. Jansson
Steven J. Hallam, Editor
Taniya Roy Chowdhury
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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  • ORCID record for Taniya Roy Chowdhury
Joon-Yong Lee
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Eric M. Bottos
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Colin J. Brislawn
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Richard Allen White III
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Lisa M. Bramer
bNational Security Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Joseph Brown
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Jeremy D. Zucker
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Young-Mo Kim
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Ari Jumpponen
cDivision of Biology, Kansas State University, Manhattan, Kansas, USA
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Charles W. Rice
cDivision of Biology, Kansas State University, Manhattan, Kansas, USA
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Sarah J. Fansler
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Thomas O. Metz
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Lee Ann McCue
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Stephen J. Callister
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Hyun-Seob Song
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Janet K. Jansson
aEarth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
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Steven J. Hallam
University of British Columbia
Roles: Editor
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DOI: 10.1128/mSystems.00061-19
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ABSTRACT

Climate change is causing shifts in precipitation patterns in the central grasslands of the United States, with largely unknown consequences on the collective physiological responses of the soil microbial community, i.e., the metaphenome. Here, we used an untargeted omics approach to determine the soil microbial community’s metaphenomic response to soil moisture and to define specific metabolic signatures of the response. Specifically, we aimed to develop the technical approaches and metabolic mapping framework necessary for future systematic ecological studies. We collected soil from three locations at the Konza Long-Term Ecological Research (LTER) field station in Kansas, and the soils were incubated for 15 days under dry or wet conditions and compared to field-moist controls. The microbiome response to wetting or drying was determined by 16S rRNA amplicon sequencing, metatranscriptomics, and metabolomics, and the resulting shifts in taxa, gene expression, and metabolites were assessed. Soil drying resulted in significant shifts in both the composition and function of the soil microbiome. In contrast, there were few changes following wetting. The combined metabolic and metatranscriptomic data were used to generate reaction networks to determine the metaphenomic response to soil moisture transitions. Site location was a strong determinant of the response of the soil microbiome to moisture perturbations. However, some specific metabolic pathways changed consistently across sites, including an increase in pathways and metabolites for production of sugars and other osmolytes as a response to drying. Using this approach, we demonstrate that despite the high complexity of the soil habitat, it is possible to generate insight into the effect of environmental change on the soil microbiome and its physiology and functions, thus laying the groundwork for future, targeted studies.

IMPORTANCE Climate change is predicted to result in increased drought extent and intensity in the highly productive, former tallgrass prairie region of the continental United States. These soils store large reserves of carbon. The decrease in soil moisture due to drought has largely unknown consequences on soil carbon cycling and other key biogeochemical cycles carried out by soil microbiomes. In this study, we found that soil drying had a significant impact on the structure and function of soil microbial communities, including shifts in expression of specific metabolic pathways, such as those leading toward production of osmoprotectant compounds. This study demonstrates the application of an untargeted multi-omics approach to decipher details of the soil microbial community’s metaphenotypic response to environmental perturbations and should be applicable to studies of other complex microbial systems as well.

  • Copyright © 2019 Roy Chowdhury et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
Taniya Roy Chowdhury, Joon-Yong Lee, Eric M. Bottos, Colin J. Brislawn, Richard Allen White III, Lisa M. Bramer, Joseph Brown, Jeremy D. Zucker, Young-Mo Kim, Ari Jumpponen, Charles W. Rice, Sarah J. Fansler, Thomas O. Metz, Lee Ann McCue, Stephen J. Callister, Hyun-Seob Song, Janet K. Jansson
mSystems Jun 2019, 4 (4) e00061-19; DOI: 10.1128/mSystems.00061-19

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Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
Taniya Roy Chowdhury, Joon-Yong Lee, Eric M. Bottos, Colin J. Brislawn, Richard Allen White III, Lisa M. Bramer, Joseph Brown, Jeremy D. Zucker, Young-Mo Kim, Ari Jumpponen, Charles W. Rice, Sarah J. Fansler, Thomas O. Metz, Lee Ann McCue, Stephen J. Callister, Hyun-Seob Song, Janet K. Jansson
mSystems Jun 2019, 4 (4) e00061-19; DOI: 10.1128/mSystems.00061-19
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KEYWORDS

metaphenome
metatranscriptome
multi-omics
soil microbiome

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