DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Sustained bacterial N2O reduction at acidic pH

Journal Article · · Nature Communications

Nitrous oxide (N2O) is a climate-active gas with emissions predicted to increase due to agricultural intensification. Microbial reduction of N2O to dinitrogen (N2) is the major consumption process but microbial N2O reduction under acidic conditions is considered negligible, albeit strongly acidic soils harbor nosZ genes encoding N2O reductase. Here, we study a co-culture derived from acidic tropical forest soil that reduces N2O at pH 4.5. The co-culture exhibits bimodal growth with a Serratia sp. fermenting pyruvate followed by hydrogenotrophic N2O reduction by a Desulfosporosinus sp. Integrated omics and physiological characterization revealed interspecies nutritional interactions, with the pyruvate fermenting Serratia sp. supplying amino acids as essential growth factors to the N2O-reducing Desulfosporosinus sp. Thus, we demonstrate growth-linked N2O reduction between pH 4.5 and 6, highlighting microbial N2O reduction potential in acidic soils.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
2471421
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (101)

LC‐MS Data Processing with MAVEN: A Metabolomic Analysis and Visualization Engine journal March 2012
Parallel‐Meta Suite: Interactive and rapid microbiome data analysis on multiple platforms journal March 2022
Effects of copper on nitrous oxide (N2O) reduction in denitrifiers and N2O emissions from agricultural soils journal September 2019
Metabolome changes are induced in the arbuscular mycorrhizal fungus Gigaspora margarita by germination and by its bacterial endosymbiont journal June 2018
The effect of pH on Marinobacter hydrocarbonoclasticus denitrification pathway and nitrous oxide reductase journal August 2020
Desulfosporosinus acidiphilus sp. nov.: a moderately acidophilic sulfate-reducing bacterium isolated from acid mining drainage sediments: New taxa: Firmicutes (Class Clostridia, Order Clostridiales, Family Peptococcaceae) journal April 2010
Desulfosporosinus acididurans sp. nov.: an acidophilic sulfate-reducing bacterium isolated from acidic sediments journal November 2014
Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity journal April 2021
Seasonal changes of CO2, CH4 and N2O fluxes in relation to land-use change in tropical peatlands located in coastal area of South Kalimantan journal July 2003
Enrichment, Cultivation, and Detection of Reductively Dechlorinating Bacteria book January 2005
Exchange of trace gases between soils and the atmosphere in Scots pine forest ecosystems of the northeastern German lowlands journal August 2002
Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane—Distinct translocases and mechanisms journal September 2008
Nitrous oxide-sink capability of denitrifying bacteria impacted by nitrite and pH journal January 2022
The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase journal June 2004
Biogeochemical Implications of N2O-Reducing Thermophilic Campylobacteria in Deep-Sea Vent Fields, and the Description of Nitratiruptor labii sp. nov. journal September 2020
The N2O product ratio of nitrification and its dependence on long-term changes in soil pH journal August 2007
Carbon and oxygen controls on N2O and N2 production during nitrate reduction journal October 2010
Spatial variation in soil pH controls off-season N2O emission in an agricultural soil journal August 2016
Nitrite kinetics during anoxia: The role of abiotic reactions versus microbial reduction journal April 2018
Soil NO3− level and O2 availability are key factors in controlling N2O reduction to N2 following long-term liming of an acidic sandy soil journal May 2019
Nitrite accumulation and impairment of N2O reduction explains contrasting soil denitrification phenotypes journal March 2022
Contrasting effects of straw and biochar on microscale heterogeneity of soil O2 and pH: Implication for N2O emissions journal March 2022
Life in acid: pH homeostasis in acidophiles journal April 2007
Genomics and Ecology of Novel N2O-Reducing Microorganisms journal January 2018
Effect of pH on N2O reduction and accumulation during denitrification by methanol utilizing denitrifiers journal October 2012
Enhancement of denitrification performance with reduction of nitrite accumulation and N2O emission by Shewanella oneidensis MR-1 in microbial denitrifying process journal February 2020
Metabolomic Analysis via Reversed-Phase Ion-Pairing Liquid Chromatography Coupled to a Stand Alone Orbitrap Mass Spectrometer journal April 2010
Inhibition of Methylmercury and Methane Formation by Nitrous Oxide in Arctic Tundra Soil Microcosms journal March 2023
Organohalide Respiration with Chlorinated Ethenes under Low pH Conditions journal July 2017
Nitrous Oxide Is a Potent Inhibitor of Bacterial Reductive Dechlorination journal December 2018
Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra journal December 2011
Refined experimental annotation reveals conserved corrinoid autotrophy in chloroform-respiring Dehalobacter isolates journal November 2016
Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms journal March 2016
Phenotypic and genotypic richness of denitrifiers revealed by a novel isolation strategy journal July 2017
Nextflow enables reproducible computational workflows journal April 2017
N2 production rates limited by nitrite availability in the Bay of Bengal oxygen minimum zone journal December 2016
How a century of ammonia synthesis changed the world journal September 2008
Fast gapped-read alignment with Bowtie 2 journal March 2012
DADA2: High-resolution sample inference from Illumina amplicon data journal May 2016
Linking meta-omics to the kinetics of denitrification intermediates reveals pH-dependent causes of N2O emissions and nitrite accumulation in soil journal July 2021
Response of N2O production rate to ocean acidification in the western North Pacific journal November 2019
The social network of microorganisms — how auxotrophies shape complex communities journal March 2018
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 journal July 2019
Effect of pH on the denitrification proteome of the soil bacterium Paracoccus denitrificans PD1222 journal August 2021
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal November 2012
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism journal November 2013
Syntrophic exchange in synthetic microbial communities journal April 2014
Networks of energetic and metabolic interactions define dynamics in microbial communities journal November 2015
Functional assembly of nitrous oxide reductase provides insights into copper site maturation journal June 2019
cblaster: a remote search tool for rapid identification and visualization of homologous gene clusters journal June 2021
Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets journal October 2013
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
fastp: an ultra-fast all-in-one FASTQ preprocessor journal September 2018
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference journal May 2019
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database journal November 2019
KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold journal November 2019
Genomic insights into a new acidophilic, copper-resistant Desulfosporosinus isolate from the oxidized tailings area of an abandoned gold mine journal May 2016
Nitrous oxide inhibition of methanogenesis represents an underappreciated greenhouse gas emission feedback journal January 2024
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
ModelTest-NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models journal August 2019
The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000 journal January 2000
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal November 2012
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies journal August 2012
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) journal November 2013
nf-core/mag: a best-practice pipeline for metagenome hybrid assembly and binning journal January 2022
Desulfosporosinus metallidurans sp. nov., an acidophilic, metal-resistant sulfate-reducing bacterium from acid mine drainage journal July 2021
DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks preprint April 2022
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
The pH dependency of N-converting enzymatic processes, pathways and microbes: effect on net N 2 O production: pH dependency of N-converting enzymatic processes, pathways and microbes journal March 2018
Competition for electrons favours N2O reduction in denitrifying Bradyrhizobium isolates journal February 2021
Enrichment and isolation of acidophilic sulfate-reducing bacteria from Tinto River sediments: Acidophilic SRB from Tinto River journal May 2013
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data journal September 2016
Strong pH influence on N 2 O and CH 4 fluxes from forested organic soils journal June 2009
Denitrification at pH 4 by a soil-derived Rhodanobacter-dominated community: Denitrification at pH 4 journal December 2010
Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century journal August 2009
Can Microscale Chemical Patches Persist in the Sea? Microelectrode Study of Marine Snow, Fecal Pellets journal February 1987
Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ journal April 2016
Metagenomic Characterization of Soil Microbial Communities in the Luquillo Experimental Forest (Puerto Rico) and Implications for Nitrogen Cycling journal May 2021
Denitrification Response Patterns during the Transition to Anoxic Respiration and Posttranscriptional Effects of Suboptimal pH on Nitrogen Oxide Reductase in Paracoccus denitrificans journal August 2010
Enhancement of Nitrous Oxide Emissions in Soil Microbial Consortia via Copper Competition between Proteobacterial Methanotrophs and Denitrifiers journal February 2021
16S rRNA Gene-Based Detection of Tetrachloroethene-Dechlorinating Desulfuromonas and Dehalococcoides Species journal April 2000
Quantitative PCR Targeting 16S rRNA and Reductive Dehalogenase Genes Simultaneously Monitors Multiple Dehalococcoides Strains journal April 2006
BtsT, a Novel and Specific Pyruvate/H+ Symporter in Escherichia coli journal October 2017
Complete Genome Sequences of Desulfosporosinus orientis DSM765T, Desulfosporosinus youngiae DSM17734T, Desulfosporosinus meridiei DSM13257T, and Desulfosporosinus acidiphilus DSM22704T journal October 2012
Mass Spectrometric Studies of the Effect of pH on the Accumulation of Intermediates in Denitrification by Paracoccus denitrificans journal February 1994
Initial Characterization of a Reductive Dehalogenase from Desulfitobacterium chlororespirans Co23. journal January 1996
Genome Sequence of the Moderately Acidophilic Sulfate-Reducing Firmicute Desulfosporosinus acididurans (Strain M1 T ) journal August 2015
Anaerobic Microbial Metabolism of Dichloroacetate journal April 2021
Impaired Reduction of N2O to N2 in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of nosZ journal June 2014
A Dual Enrichment Strategy Provides Soil- and Digestate-Competent Nitrous Oxide-Respiring Bacteria for Mitigating Climate Forcing in Agriculture journal June 2022
Influence of interfaces on microbial activity journal March 1990
Clarifying Microbial Nitrous Oxide Reduction under Aerobic Conditions: Tolerant, Intolerant, and Sensitive journal April 2023
BLAST+: architecture and applications journal January 2009
Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction journal June 2012
Singularity: Scientific containers for mobility of compute journal May 2017
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Anoxic growth of Ensifer meliloti 1021 by N2O-reduction, a potential mitigation strategy journal May 2015
Compilation of Henry's law constants (version 4.0) for water as solvent journal January 2015
Coupled abiotic-biotic cycling of nitrous oxide in tropical peatlands dataset January 2022
The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes preprint March 2016
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies journal January 2019