Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations.

Taniya Roy Chowdhury,Charles W Rice,Jeremy D Zucker,Ari Jumpponen,Joon-Yong Lee,Lisa M Bramer,Hyun-Seob Song,Young-Mo Kim,Thomas O Metz,Janet K Jansson,Richard Allen White,Eric M Bottos,Lee Ann Mccue,Joseph Brown,Stephen J Callister,Sarah J Fansler,Colin J Brislawn

doi:10.1128/msystems.00061-19

Taniya Roy Chowdhury, Charles W Rice + Show 15 more

Open Access

https://doi.org/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.

Highlights

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
Native prairie soils were collected in triplicate from three field locations across a landscape gradient at the Konza Long-Term Ecological Research (LTER) site in Kansas [11]
By multivariate statistical analysis of the 16S data, we found that soil drying had a significant impact on bacterial ␤-diversity, as shown on the second axis of the nonmetric multidimensional scaling (NMDS) plot, which clearly separates all of the dried samples from the rest (Fig. 1a)

Summary

Introduction

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. 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, laying the groundwork for future, targeted studies. As precipitation regimes with fewer, but larger, events amplify fluctuations in soil water content, the consequences in mesic grassland ecosystems will be prolonged dry periods between rainfall events and an increase in the length and occurrence of drought stress [4] These grassland soils store large amounts of carbon, up to 39% of the organic carbon stocks in the conterminous United States [5], and the fate of this stored C is uncertain as climate changes. A critical knowledge gap exists about how indigenous, active, and naturally interacting members of soil microbial communities respond to changes in soil moisture by changing levels of gene expression, as measured by metatranscriptomics (MT)

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