Rapid Response of Nitrogen Cycling Gene Transcription to Labile Carbon Amendments in a Soil Microbial Community

Peter F Chuckran; Viacheslav Fofanov; Bruce A Hungate; Ember M Morrissey; Egbert Schwartz; Jeth Walkup; Paul Dijkstra

doi:10.1128/mSystems.00161-21

Rapid Response of Nitrogen Cycling Gene Transcription to Labile Carbon Amendments in a Soil Microbial Community

mSystems. 2021 May 11;6(3):e00161-21. doi: 10.1128/mSystems.00161-21.

Authors

Peter F Chuckran^{1

2}, Viacheslav Fofanov^{3

4}, Bruce A Hungate^{5

2}, Ember M Morrissey⁶, Egbert Schwartz^{5

2}, Jeth Walkup⁶, Paul Dijkstra^{5

2}

Affiliations

¹ Center for Ecosystem Science and Society (ECOSS), Northern Arizona University, Flagstaff, Arizona, USA pfchuckran@gmail.com.
² Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA.
³ Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA.
⁴ School of Informatics, Computing and Cyber Systems, Northern Arizona University, Flagstaff, Arizona, USA.
⁵ Center for Ecosystem Science and Society (ECOSS), Northern Arizona University, Flagstaff, Arizona, USA.
⁶ Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, USA.

Abstract

Episodic inputs of labile carbon (C) to soil can rapidly stimulate nitrogen (N) immobilization by soil microorganisms. However, the transcriptional patterns that underlie this process remain unclear. In order to better understand the regulation of N cycling in soil microbial communities, we conducted a 48-h laboratory incubation with agricultural soil where we stimulated the uptake of inorganic N by amending the soil with glucose. We analyzed the metagenome and metatranscriptome of the microbial communities at four time points that corresponded with changes in N availability. The relative abundances of genes remained largely unchanged throughout the incubation. In contrast, glucose addition rapidly increased the transcription of genes encoding ammonium and nitrate transporters, enzymes responsible for N assimilation into biomass, and genes associated with the N regulatory network. This upregulation coincided with an increase in transcripts associated with glucose breakdown and oxoglutarate production, demonstrating a connection between C and N metabolism. When concentrations of ammonium were low, we observed a transient upregulation of genes associated with the nitrogen-fixing enzyme nitrogenase. Transcripts for nitrification and denitrification were downregulated throughout the incubation, suggesting that dissimilatory transformations of N may be suppressed in response to labile C inputs in these soils. These results demonstrate that soil microbial communities can respond rapidly to changes in C availability by drastically altering the transcription of N cycling genes.IMPORTANCE A large portion of activity in soil microbial communities occurs in short time frames in response to an increase in C availability, affecting the biogeochemical cycling of nitrogen. These changes are of particular importance as nitrogen represents both a limiting nutrient for terrestrial plants as well as a potential pollutant. However, we lack a full understanding of the short-term effects of labile carbon inputs on the metabolism of microbes living in soil. Here, we found that soil microbial communities responded to labile carbon addition by rapidly transcribing genes encoding proteins and enzymes responsible for inorganic nitrogen acquisition, including nitrogen fixation. This work demonstrates that soil microbial communities respond within hours to carbon inputs through altered gene expression. These insights are essential for an improved understanding of the microbial processes governing soil organic matter production, decomposition, and nutrient cycling in natural and agricultural ecosystems.

Keywords: carbon metabolism; metagenomics; metatranscriptomics; microbial ecology; nitrogen fixation; nitrogen metabolism; nitrogen regulation; nutrient transport; soil microbiology.