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Title: Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations

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 microbiomemore » 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. 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.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [2];  [2];  [1]; ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Kansas State Univ., Manhattan, KS (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1530883
Report Number(s):
PNNL-SA-129510
Journal ID: ISSN 2379-5077
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; metaphenome; metatranscriptome; multi-omics; soil microbiome

Citation Formats

Roy Chowdhury, Taniya, Lee, Joon-Yong, Bottos, Eric M., Brislawn, Colin J., White, Richard Allen, Bramer, Lisa M., Brown, Joseph M., Zucker, Jeremy D., Kim, Young-Mo, Jumpponen, Ari, Rice, Charles W., Fansler, Sarah J., Metz, Thomas O., McCue, Lee Ann, Callister, Stephen J., Song, Hyun-Seob, and Jansson, Janet K. Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations. United States: N. p., 2019. Web. doi:10.1128/MsYSTEMS.00061-19.
Roy Chowdhury, Taniya, Lee, Joon-Yong, Bottos, Eric M., Brislawn, Colin J., White, Richard Allen, Bramer, Lisa M., Brown, Joseph M., Zucker, Jeremy D., Kim, Young-Mo, Jumpponen, Ari, Rice, Charles W., Fansler, Sarah J., Metz, Thomas O., McCue, Lee Ann, Callister, Stephen J., Song, Hyun-Seob, & Jansson, Janet K. Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations. United States. https://doi.org/10.1128/MsYSTEMS.00061-19
Roy Chowdhury, Taniya, Lee, Joon-Yong, Bottos, Eric M., Brislawn, Colin J., White, Richard Allen, Bramer, Lisa M., Brown, Joseph M., Zucker, Jeremy D., Kim, Young-Mo, Jumpponen, Ari, Rice, Charles W., Fansler, Sarah J., Metz, Thomas O., McCue, Lee Ann, Callister, Stephen J., Song, Hyun-Seob, and Jansson, Janet K. Tue . "Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations". United States. https://doi.org/10.1128/MsYSTEMS.00061-19. https://www.osti.gov/servlets/purl/1530883.
@article{osti_1530883,
title = {Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations},
author = {Roy Chowdhury, Taniya and Lee, Joon-Yong and Bottos, Eric M. and Brislawn, Colin J. and White, Richard Allen and Bramer, Lisa M. and Brown, Joseph M. and Zucker, Jeremy D. and Kim, Young-Mo and Jumpponen, Ari and Rice, Charles W. and Fansler, Sarah J. and Metz, Thomas O. and McCue, Lee Ann and Callister, Stephen J. and Song, Hyun-Seob and Jansson, Janet K.},
abstractNote = {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. 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.},
doi = {10.1128/MsYSTEMS.00061-19},
journal = {mSystems},
number = 4,
volume = 4,
place = {United States},
year = {Tue Jun 11 00:00:00 EDT 2019},
month = {Tue Jun 11 00:00:00 EDT 2019}
}

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Works referenced in this record:

Microbial Community Structure and Functional Potential in Cultivated and Native Tallgrass Prairie Soils of the Midwestern United States
journal, August 2018

  • Mackelprang, Rachel; Grube, Alyssa M.; Lamendella, Regina
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01775

Regional grassland productivity responses to precipitation during multiyear above- and below-average rainfall periods
journal, February 2018

  • Petrie, Matthew D.; Peters, Debra P. C.; Yao, Jin
  • Global Change Biology, Vol. 24, Issue 5
  • DOI: 10.1111/gcb.14024

Pathview: an R/Bioconductor package for pathway-based data integration and visualization
journal, June 2013


Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
journal, April 2014

  • Taş, Neslihan; Prestat, Emmanuel; McFarland, Jack W.
  • The ISME Journal, Vol. 8, Issue 9
  • DOI: 10.1038/ismej.2014.36

Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation
journal, February 2014


GAGE: generally applicable gene set enrichment for pathway analysis
journal, January 2009


iPath3.0: interactive pathways explorer v3
journal, April 2018

  • Darzi, Youssef; Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky299

Differential sensitivity to regional-scale drought in six central US grasslands
journal, February 2015


Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales
journal, October 2013

  • Zeglin, L. H.; Bottomley, P. J.; Jumpponen, A.
  • Ecology, Vol. 94, Issue 10
  • DOI: 10.1890/12-2018.1

The immediate and prolonged effects of climate extremes on soil respiration in a mesic grassland: Soil Respiration and Climate Extremes
journal, April 2016

  • Hoover, David L.; Knapp, Alan K.; Smith, Melinda D.
  • Journal of Geophysical Research: Biogeosciences, Vol. 121, Issue 4
  • DOI: 10.1002/2015JG003256

Comparison of Sequencing Utility Programs
journal, January 2013


A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning
journal, September 2011


Effect of Water-Filled Pore Space on Carbon Dioxide and Nitrous Oxide Production in Tilled and Nontilled Soils1
journal, January 1984


Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms
journal, April 2015


Metabolic Responses of Poplar to Apripona germari (Hope) as Revealed by Metabolite Profiling
journal, June 2016

  • Wang, Lijuan; Qu, Liangjian; Zhang, Liwei
  • International Journal of Molecular Sciences, Vol. 17, Issue 6
  • DOI: 10.3390/ijms17060923

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

Biogeography and organic matter removal shape long-term effects of timber harvesting on forest soil microbial communities
journal, July 2017

  • Wilhelm, Roland C.; Cardenas, Erick; Maas, Kendra R.
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.109

Atmospheric circulation anomalies during two persistent north american droughts: 1932–1939 and 1948–1957
journal, April 2010


MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
journal, May 2016


Stimulation of Different Functional Groups of Bacteria by Various Plant Residues as a Driver of Soil Priming Effect
journal, February 2013


Altered Rainfall Patterns, Gas Exchange, and Growth in Grasses and Forbs
journal, July 2002

  • Fay, Philip A.; Carlisle, Jonathan D.; Danner, Brett T.
  • International Journal of Plant Sciences, Vol. 163, Issue 4
  • DOI: 10.1086/339718

Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes
journal, July 2017

  • Santos-Medellín, Christian; Edwards, Joseph; Liechty, Zachary
  • mBio, Vol. 8, Issue 4
  • DOI: 10.1128/mBio.00764-17

Fluxes of CO2 From Grazed and Ungrazed Tallgrass Prairie
journal, March 2006

  • Owensby, Clenton E.; Ham, Jay M.; Auen, Lisa M.
  • Rangeland Ecology & Management, Vol. 59, Issue 2
  • DOI: 10.2111/05-116R2.1

Improved quality control processing of peptide-centric LC-MS proteomics data
journal, August 2011


Not all droughts are created equal: the impacts of interannual drought pattern and magnitude on grassland carbon cycling
journal, February 2016

  • Hoover, David L.; Rogers, Brendan M.
  • Global Change Biology, Vol. 22, Issue 5
  • DOI: 10.1111/gcb.13161

The soil microbiome — from metagenomics to metaphenomics
journal, June 2018


Ribosomal Database Project: data and tools for high throughput rRNA analysis
journal, November 2013

  • Cole, James R.; Wang, Qiong; Fish, Jordan A.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1244

Actinobacteria from Arid and Desert Habitats: Diversity and Biological Activity
journal, January 2016


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Leakage-free rapid quenching technique for yeast metabolomics
journal, June 2008


A communal catalogue reveals Earth’s multiscale microbial diversity
journal, November 2017

  • Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel
  • Nature, Vol. 551, Issue 7681
  • DOI: 10.1038/nature24621

Climate-Driven Interannual Variability in Net Ecosystem Exchange in the Northern Great Plains Grasslands
journal, January 2010

  • Zhang, Li; Wylie, Bruce K.; Ji, Lei
  • Rangeland Ecology & Management, Vol. 63, Issue 1
  • DOI: 10.2111/08-232.1

Vertical distribution of fungal communities in tallgrass prairie soil
journal, September 2010

  • Jumpponen, Ari; Jones, Kenneth L.; Blair, John
  • Mycologia, Vol. 102, Issue 5
  • DOI: 10.3852/09-316

Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought
journal, November 2012

  • Bouskill, Nicholas J.; Lim, Hsiao Chien; Borglin, Sharon
  • The ISME Journal, Vol. 7, Issue 2
  • DOI: 10.1038/ismej.2012.113

Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes
journal, June 2016


MetaPathways v2.5: quantitative functional, taxonomic and usability improvements: Fig. 1.
journal, June 2015


Consequences of More Extreme Precipitation Regimes for Terrestrial Ecosystems
journal, October 2008

  • Knapp, Alan K.; Beier, Claus; Briske, David D.
  • BioScience, Vol. 58, Issue 9
  • DOI: 10.1641/B580908

Altering Rainfall Timing and Quantity in a Mesic Grassland Ecosystem: Design and Performance of Rainfall Manipulation Shelters
journal, May 2000

  • Fay, Philip A.; Carlisle, Jonathan D.; Knapp, Alan K.
  • Ecosystems, Vol. 3, Issue 3
  • DOI: 10.1007/s100210000028

Controls of Aboveground Net Primary Production in Mesic Savanna Grasslands: An Inter-Hemispheric Comparison
journal, September 2009


Effects of drought and N-fertilization on N cycling in two grassland soils
journal, January 2013


A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land
journal, November 2008

  • Battistuzzi, F. U.; Hedges, S. B.
  • Molecular Biology and Evolution, Vol. 26, Issue 2
  • DOI: 10.1093/molbev/msn247

Superstatistics of hydro-climatic fluctuations and interannual ecosystem productivity
journal, January 2006

  • Porporato, Amilcare; Vico, Giulia; Fay, Philip A.
  • Geophysical Research Letters, Vol. 33, Issue 15
  • DOI: 10.1029/2006GL026412

Correction to “Upscaling carbon fluxes over the Great Plains grasslands: Sinks and sources”
journal, January 2011

  • Zhang, Li; Wylie, Bruce K.; Ji, Lei
  • Journal of Geophysical Research, Vol. 116, Issue G3
  • DOI: 10.1029/2011JG001832

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry
journal, December 2009

  • Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup
  • Analytical Chemistry, Vol. 81, Issue 24
  • DOI: 10.1021/ac9019522

Analysis of Factors Controlling Soil Carbon in the Conterminous United States
journal, January 2006

  • Guo, Yinyan; Gong, Peng; Amundson, Ronald
  • Soil Science Society of America Journal, Vol. 70, Issue 2
  • DOI: 10.2136/sssaj2005.0163

Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem
journal, February 2005


Afternoon rain more likely over drier soils
journal, September 2012

  • Taylor, Christopher M.; de Jeu, Richard A. M.; Guichard, Françoise
  • Nature, Vol. 489, Issue 7416
  • DOI: 10.1038/nature11377

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009

  • Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
  • Analytical Chemistry, Vol. 81, Issue 9
  • DOI: 10.1021/ac802689c

Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
journal, January 1995


Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?
journal, September 2011


Reconciling inconsistencies in precipitation-productivity relationships: implications for climate change
journal, December 2016

  • Knapp, Alan K.; Ciais, Philippe; Smith, Melinda D.
  • New Phytologist, Vol. 214, Issue 1
  • DOI: 10.1111/nph.14381

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Linking soil biology and chemistry in biological soil crust using isolate exometabolomics
journal, January 2018


Drought and host selection influence bacterial community dynamics in the grass root microbiome
journal, July 2017

  • Naylor, Dan; DeGraaf, Stephanie; Purdom, Elizabeth
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.118

Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021


Aging features of the migratory locust at physiological and transcriptional levels
journal, April 2021


Improved quality control processing of peptide-centric LC-MS proteomics data
text, January 2011

  • G., Pounds, Joel; C., Sims, Amy; O., Metz, Thomas
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/kpz0-8g92

Fluxes of CO2 From Grazed and Ungrazed Tallgrass Prairie
journal, January 2006


Effects of drought and N-fertilization on N cycling in two grassland soils
text, January 2013

  • Hartmann, Adrian A.; Barnard, Romain L.; Marhan, Sven
  • Springer
  • DOI: 10.5167/uzh-82173

Atmospheric circulation anomalies during two persistent north american droughts: 1932-1939 and 1948-1957
text, January 2011

  • Cook, Benjamin I.; Seager, Richard; Miller, Ronald L.
  • Columbia University
  • DOI: 10.7916/d8c53wbj

A communal catalogue reveals Earths multiscale microbial diversity
text, January 2017


Effects of drought and N-fertilization on N cycling in two grassland soils
text, January 2013


A communal catalogue reveals Earth's multiscale microbial diversity
dataset, November 2017

  • Thompson, Luke; Sanders, Jon; McDonald, Daniel
  • Zenodo, 33 files (CSV, TSV, BIOM, TXT, GZ, RDB); 47.3 GB
  • DOI: 10.5281/zenodo.889999

MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
text, January 2016

  • Bobbie-Jo, Webb-Robertson,; D., Smith, Richard; S., Nakayasu, Ernesto
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/xw6w-ts66

Works referencing / citing this record:

Soil microbiomes and climate change
journal, October 2019