skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · mSystems
ORCiD logo [1];  [2]; ORCiD logo [1];  [3];  [1];  [3];  [1];
  1. Center for Ecosystem Science and Society (ECOSS), Northern Arizona University, Flagstaff, Arizona, USA, Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
  2. Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA, School of Informatics, Computing and Cyber Systems, Northern Arizona University, Flagstaff, Arizona, USA
  3. Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, USA

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.

Research Organization:
Univ. of California, Oakland, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SCW1632; AC02-05CH11231
OSTI ID:
1782385
Alternate ID(s):
OSTI ID: 1816183
Journal Information:
mSystems, Journal Name: mSystems Vol. 6 Journal Issue: 3; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (80)

Genetic regulation of nitrogen metabolism in the fungi. journal January 1997
Determining potential glutamine synthetase and glutamate dehydrogenase activity in soil journal August 2009
Glucose triggers strong taxon‐specific responses in microbial growth and activity: insights from DNA and RNA qSIP journal November 2019
Maintenance carbon requirements of actively-metabolizing microbial populations under in situ conditions journal January 1985
Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB journal February 2002
The effects of glucose loading rates on bacterial and fungal growth in soil journal March 2014
Differential Assemblage of Functional Units in Paddy Soil Microbiomes journal April 2015
Orchestrating high-throughput genomic analysis with Bioconductor journal January 2015
Manipulating nitrogen regulation in diazotrophic bacteria for agronomic benefit journal April 2019
Priming effects: Interactions between living and dead organic matter journal September 2010
Development of a diverse epiphyte community in response to phosphorus fertilization journal July 2007
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
Nitrogen Assimilation in Escherichia coli: Putting Molecular Data into a Systems Perspective journal December 2013
Pathways of nitrogen utilization by soil microorganisms – A review journal December 2010
ggplot2 book January 2016
Active and total microbial communities in forest soil are largely different and highly stratified during decomposition journal July 2011
The Emergence of 2-Oxoglutarate as a Master Regulator Metabolite journal September 2015
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
Nitrogen regulatory protein C-controlled genes of Escherichia coli: Scavenging as a defense against nitrogen limitation journal December 2000
Modeling soil metabolic processes using isotopologue pairs of position-specific 13C-labeled glucose and pyruvate journal September 2011
Purification and properties of NADP-dependent glutamate dehydrogenase from Ruminococcus flavefaciens FD-1. journal January 1992
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources journal January 2014
How Plant Root Exudates Shape the Nitrogen Cycle journal August 2017
Microbial hotspots and hot moments in soil: Concept & review journal April 2015
Nutrient Acquisition, Rather Than Stress Response Over Diel Cycles, Drives Microbial Transcription in a Hyper-Arid Namib Desert Soil journal May 2019
Rewetting of soil: Revisiting the origin of soil CO2 emissions journal August 2020
The nitrogen cycle journal February 2016
Metagenomes and Metatranscriptomes of a Glucose-Amended Agricultural Soil journal October 2020
Niche differentiation is spatially and temporally regulated in the rhizosphere journal January 2020
Metabolomics‐driven quantitative analysis of ammonia assimilation in E. coli journal January 2009
Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? journal February 1996
A survey of best practices for RNA-seq data analysis journal January 2016
Role of NAD-linked glutamate dehydrogenase in nitrogen metabolism in Saccharomyces cerevisiae. journal September 1990
Complete nitrification by Nitrospira bacteria journal November 2015
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
Land Use Type Significantly Affects Microbial Gene Transcription in Soil journal February 2014
Linking soil bacterial biodiversity and soil carbon stability journal October 2014
The control of nitrous oxide emissions from agricultural and natural soils journal July 2000
Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates journal January 2013
In a class of its own ? the RNA polymerase sigma factor ?; 54 (? N ) journal December 1993
Application of metatranscriptomics to soil environments journal November 2012
Available C and N affect the utilization of glycine by soil microorganisms journal December 2016
Microbial expression profiles in the rhizosphere of two maize lines differing in N use efficiency journal October 2018
Ecological importance of soil bacterivores for ecosystem functions journal September 2015
Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil journal January 1985
Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment journal January 2009
Complete nitrification by a single microorganism journal November 2015
The activity level of a microbial community function can be predicted from its metatranscriptome journal November 2011
The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review journal January 2005
Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter: Seasonal dynamics of a soil microbial community journal October 2015
Changes in Denitrifier Abundance, Denitrification Gene mRNA Levels, Nitrous Oxide Emissions, and Denitrification in Anoxic Soil Microcosms Amended with Glucose and Plant Residues journal February 2010
Nitrogen Assimilation and Global Regulation in Escherichia coli journal October 2003
Evolution of Nitrate Reductase: Molecular and Structural Variations on a Common Function journal March 2002
Metatranscriptomics reveals climate change effects on the rhizosphere microbiomes in European grassland journal November 2019
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model journal April 2003
Pasture in crop rotations influences microbial biodiversity and function reducing the potential for nitrogen loss from compost journal December 2020
The Nitrate Assimilatory Pathway in Sinorhizobium meliloti: Contribution to NO Production journal July 2019
KEGG Mapper for inferring cellular functions from protein sequences journal August 2019
Induced N-limitation of bacterial growth in soil: Effect of carbon loading and N status in soil journal July 2014
Short-Term Transcriptional Response of Microbial Communities to Nitrogen Fertilization in a Pine Forest Soil journal May 2018
Denitrification: ecological niches, competition and survival journal January 1983
Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: A global assessment journal August 2006
Coordination of microbial metabolism journal March 2014
Threshold concentration of glucose for bacterial growth in soil journal January 2015
Genetic regulation of biological nitrogen fixation journal August 2004
Regulation of extracellular protease activity in soil in response to different sources and concentrations of nitrogen and carbon journal December 2008
Comparison of factors limiting bacterial growth in different soils journal October 2007
Stimulation of heterotrophic nitrification and N2O production, inhibition of autotrophic nitrification in soil by adding readily degradable carbon journal August 2019
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes journal October 2018
Metatranscriptomics Reveals the Diversity of Genes Expressed by Eukaryotes in Forest Soils journal January 2012
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates journal November 2013
Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems journal July 2013
Metatranscriptomics: Eavesdropping on Complex Microbial Communities journal July 2009
Competition for Ammonium between Nitrifying and Heterotrophic Bacteria in Continuously Percolated Soil Columns journal January 1992
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed journal February 2008
Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates journal April 2015
Soil Health Indicators during Transition from Row Crops to Grass-Legume Sod journal November 2017
Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling journal April 2014
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Apparent negative co-operativity and substrate inhibition in overexpressed glutamate dehydrogenase from Escherichia coli: Negative co-operativity in E. coli glutamate dehydrogenase journal April 2008