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 determ...

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Autores principales:	Taniya Roy Chowdhury, Joon-Yong Lee, Eric M. Bottos, Colin J. Brislawn, Richard Allen White, 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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	metaphenome metatranscriptome multi-omics soil microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/47047ddab7ff4fd997a736f630733e1b
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spelling	oai:doaj.org-article:47047ddab7ff4fd997a736f630733e1b2021-12-02T18:39:47ZMetaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations10.1128/mSystems.00061-192379-5077https://doaj.org/article/47047ddab7ff4fd997a736f630733e1b2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00061-19https://doaj.org/toc/2379-5077ABSTRACT 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.Taniya Roy ChowdhuryJoon-Yong LeeEric M. BottosColin J. BrislawnRichard Allen WhiteLisa M. BramerJoseph BrownJeremy D. ZuckerYoung-Mo KimAri JumpponenCharles W. RiceSarah J. FanslerThomas O. MetzLee Ann McCueStephen J. CallisterHyun-Seob SongJanet K. JanssonAmerican Society for Microbiologyarticlemetaphenomemetatranscriptomemulti-omicssoil microbiomeMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	metaphenome metatranscriptome multi-omics soil microbiome Microbiology QR1-502
spellingShingle	metaphenome metatranscriptome multi-omics soil microbiome Microbiology QR1-502 Taniya Roy Chowdhury Joon-Yong Lee Eric M. Bottos Colin J. Brislawn Richard Allen White 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 Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
description	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.
format	article
author	Taniya Roy Chowdhury Joon-Yong Lee Eric M. Bottos Colin J. Brislawn Richard Allen White 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
author_facet	Taniya Roy Chowdhury Joon-Yong Lee Eric M. Bottos Colin J. Brislawn Richard Allen White 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
author_sort	Taniya Roy Chowdhury
title	Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
title_short	Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
title_full	Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
title_fullStr	Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
title_full_unstemmed	Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
title_sort	metaphenomic responses of a native prairie soil microbiome to moisture perturbations
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/47047ddab7ff4fd997a736f630733e1b
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Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations

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