Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Floodplain nitrifiers harbor the genetic potential for utilizing a wide range of organic nitrogen compounds

Journal Article · · mSystems
 [1];  [2];  [2];  [2];  [2];  [2];  [3];  [1];  [2]
  1. SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  2. Stanford Univ., CA (United States)
  3. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Organic compounds such as urea and cyanate can serve as nitrogen (N) sources for nitrifying microorganisms, including ammonia-oxidizing archaea (AOA) and bacteria (AOB), complete ammonia-oxidizing (comammox) bacteria, and nitrite-oxidizing bacteria (NOB). Here we investigated metagenome-assembled genomes (MAGs) for all four nitrifier guilds generated from hydrologically variable floodplain sediments of the Wind River Basin (WRB; Riverton, WY, USA) for their genetic potential to utilize organic N compounds. A vast majority of WRB nitrifier MAGs harbored urease (ure) and at least one urea transporter (utp, urt, dur3). AOA were the most abundant and phylogenetically diverse nitrifiers in WRB floodplain sediments. Several AOA MAGs encoded cyanase (cynS), nitrilase (nit1), omega-amidase (nit2), nitrile hydratase (nthA), and genes related to purine degradation, including biuret hydrolase (biuH), oxamic transcarbamylase (allFGH), and catabolic carbamate kinase (allK). AOA often encoded an uncharacterized amidohydrolase collocated with biuH, rather than allophanate hydrolase (atzF). A small number of AOA encoded atzF, functioning in an unknown pathway. AOB and comammox were of relatively low abundance and taxonomic diversity and were present only at certain depths in WRB; however, they encoded triuret/biuret degradation genes (trtA, biuH, and atzH), and in comammox, these genes were also collocated with allFGHK. The genetic potential of ammonia oxidizers in the WRB floodplain suggests that organic N may support nitrification in this system. The proposed pathways for utilizing purine degradation products other than urea potentially expand the known metabolic capabilities of AOA, AOB, and comammox bacteria and reveal the possibility for cryptic N cycling between microbial community members.

Research Organization:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0019119; AC02-76SF00515; AC02-05CH11231
OSTI ID:
3000948
Journal Information:
mSystems, Journal Name: mSystems Journal Issue: 11 Vol. 10; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (131)

An extension of the flood pulse concept journal January 2000
Hyporheic flow and transport processes: Mechanisms, models, and biogeochemical implications: HYPORHEIC FLOW AND TRANSPORT PROCESSES journal October 2014
Hot Spots and Hot Moments of Nitrogen in a Riparian Corridor journal January 2018
Microbial oxidation of nitrogen supplied as selected organic nitrogen compounds in the South Atlantic Bight journal December 2018
Dynamics of leaf litter accumulation and its effects on riparian vegetation: A review journal July 1997
Diverse Thaumarchaeota Dominate Subsurface Ammonia-oxidizing Communities in Semi-arid Floodplains in the Western United States journal June 2020
Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor journal November 2013
Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems journal June 2003
Hydrogeomorphology Influences Soil Nitrogen and Phosphorus Mineralization in Floodplain Wetlands journal September 2012
Active methane processing microbes and the disproportionate role of NC10 phylum in methane mitigation in Amazonian floodplains journal September 2021
Ureide metabolism in plant-associated bacteria: purine plant-bacteria interactive scenarios under nitrogen deficiency journal May 2018
Allantoin: Emerging Role in Plant Abiotic Stress Tolerance journal January 2021
Refining the site conceptual model at a former uranium mill site in Riverton, Wyoming, USA journal July 2015
Release of Nutrients and Organic Matter from River Floodplain Habitats: Simulating Seasonal Inundation Dynamics journal June 2013
Determination of cyanate, and a study of its accumulation in aqueous solutions of urea journal March 1964
Purine catabolism by enterobacteria book December 2022
Triuret: a novel product of peroxynitrite-mediated oxidation of urate journal March 2004
Cyanate dynamics under algal blooms and sediment resuspension events in a shallow micro-tidal estuary in the lower Chesapeake Bay journal February 2023
Contaminant mobilization from the vadose zone to groundwater during experimental river flooding events journal July 2024
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences journal February 2016
Understanding controls on redox processes in floodplain sediments of the Upper Colorado River Basin journal December 2017
An exploration of manure derived N in soils using 15N after the application of biochar, straw and a mix of both journal January 2022
Extending the benefits of PGPR to bioremediation of nitrile pollution in crop lands for enhancing crop productivity journal June 2022
Soil microbial organic nitrogen uptake is regulated by carbon availability journal October 2014
Variability of the transporter gene complement in ammonia-oxidizing archaea journal December 2014
A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria journal September 2016
The biochemistry of nitrogen mobilization: purine ring catabolism journal July 2011
Uranium storage mechanisms in wet-dry redox cycled sediments journal April 2019
The ammonification and nitrification in soil of urea with and without biuret journal October 1970
Water Table Dynamics and Biogeochemical Cycling in a Shallow, Variably-Saturated Floodplain journal March 2017
Redox Controls over the Stability of U(IV) in Floodplains of the Upper Colorado River Basin journal September 2017
Distribution, Sources, and Sinks of Cyanate in the Coastal North Atlantic Ocean journal June 2016
Controlled release fertilizers by chemical modification of urea. Triuret journal May 1973
Domain-specific recruitment of amide amino acids for protein synthesis journal September 2000
Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms journal January 2011
Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines journal December 2015
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication journal July 2017
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria journal September 2009
Cyanate as an energy source for nitrifiers journal July 2015
Complete nitrification by a single microorganism journal November 2015
Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle journal August 2017
Fast gapped-read alignment with Bowtie 2 journal March 2012
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions journal January 2018
Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea journal July 2020
Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages journal April 2021
Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities journal July 2021
Diverse ecophysiological adaptations of subsurface Thaumarchaeota in floodplain sediments revealed through genome-resolved metagenomics journal December 2021
Nitrification and beyond: metabolic versatility of ammonia oxidising archaea journal July 2023
Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes journal April 2018
Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean journal February 2020
Gene duplication drives genome expansion in a major lineage of Thaumarchaeota journal October 2020
Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment journal December 2018
Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences journal January 2024
New insights from uncultivated genomes of the global human gut microbiome journal March 2019
Growth of complete ammonia oxidizers on guanidine journal August 2024
Carbamoyl phosphate and its substitutes for the uracil synthesis in origins of life scenarios journal September 2021
Molecular diversity of dissolved organic matter reflects macroecological patterns in river networks journal July 2025
Cyanate is a low abundance but actively cycled nitrogen compound in soil journal August 2021
The fumarylacetoacetate hydrolase (FAH) superfamily of enzymes: multifunctional enzymes from microbes to mitochondria journal February 2018
The isomeric transformation of urea into ammonium cyanate in aqueous solutions journal January 1948
Mineralisation and nitrification of biuret and urea nitrogen in two New Zealand forest soils journal August 2022
Role for urea in nitrification by polar marine Archaea journal October 2012
Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira journal August 2015
Old enzymes versus new herbicides journal May 2018
Aquifex aeolicus Aspartate Transcarbamoylase, an Enzyme Specialized for the Efficient Utilization of Unstable Carbamoyl Phosphate at Elevated Temperature journal October 2003
Discovery of an ultraspecific triuret hydrolase (TrtA) establishes the triuret biodegradation pathway journal January 2021
Reactions of Peroxynitrite with Uric Acid: Formation of Reactive Intermediates, Alkylated Products and Triuret, and In Vivo Production of Triuret Under Conditions of Oxidative Stress journal March 2009
The Isolation, Characterization, and Identification of the Crystalline Inclusions of the Large Free-Living Amebae journal April 1960
From legacy contamination to watershed systems science: a review of scientific insights and technologies developed through DOE-supported research in water and energy security journal March 2022
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets journal October 2015
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database journal November 2019
Predicting gene distribution in ammonia-oxidizing archaea using phylogenetic signals journal January 2025
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era journal February 2020
eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale journal October 2021
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool journal April 2024
KEGG: biological systems database as a model of the real world journal October 2024
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
SimpleSynteny: a web-based tool for visualization of microsynteny across multiple species journal May 2016
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses journal November 2018
Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota journal June 2014
Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean preprint February 2019
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Archaea produce lower yields of N 2 O than bacteria during aerobic ammonia oxidation in soil : N journal April 2016
Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities: Oxidation of urea-derived nitrogen in the sea journal August 2016
Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily journal March 2018
Metagenome‐Assembled Genomes for Oligotrophic Nitrifiers From a Mountainous Gravelbed Floodplain journal March 2025
Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms journal May 2008
Archaea rather than bacteria control nitrification in two agricultural acidic soils: Archaeal nitrification in acidic soils journal October 2010
Hot Spots and Hot Moments in Riparian Zones: Potential for Improved Water Quality Management 1 : H journal March 2010
Not just a methane source: Amazonian floodplain sediments harbour a high diversity of methanotrophs with different metabolic capabilities journal April 2021
Global niche partitioning of purine and pyrimidine cross-feeding among ocean microbes journal January 2025
Enrichment and Physiological Characterization of a Novel Nitrospira -Like Bacterium Obtained from a Marine Sponge journal July 2010
Cyanuric Acid Biodegradation via Biuret: Physiology, Taxonomy, and Geospatial Distribution journal January 2020
Transcriptional Response of the Archaeal Ammonia Oxidizer Nitrosopumilus maritimus to Low and Environmentally Relevant Ammonia Concentrations journal August 2013
Responses of Ammonia-Oxidizing Bacterial and Archaeal Populations to Organic Nitrogen Amendments in Low-Nutrient Groundwater journal February 2010
Filling in the Gaps in Metformin Biodegradation: a New Enzyme and a Metabolic Pathway for Guanylurea journal May 2021
Urease-Encoding Genes in Ammonia-Oxidizing Bacteria journal April 2004
Allophanate Hydrolase, Not Urease, Functions in Bacterial Cyanuric Acid Metabolism journal August 2005
Oxamic transcarbamylase of Escherichia coli is encoded by the three genes allFGH (formerly fdrA, ylbE , and ylbF ) journal July 2024
Competition between ammonia-oxidizing archaea and complete ammonia oxidizers from freshwater environments journal February 2024
Degradation of purines and pyrimidines by microorganisms journal June 1976
It Takes a Village: Microbial Communities Thrive through Interactions and Metabolic Handoffs journal March 2018
Metabolite diversity among representatives of divergent Prochlorococcus ecotypes journal October 2023
Nitrogen source influences the interactions of comammox bacteria with aerobic nitrifiers journal May 2024
The Chemistry and Metabolism of the Nucleic Acids, Purines, and Pyrimidines journal June 1933
THE ECOLOGY OF INTERFACES:Riparian Zones journal November 1997
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis journal September 2018
Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale journal May 2021
Structural and biochemical characterization of the biuret hydrolase (BiuH) from the cyanuric acid catabolism pathway of Rhizobium leguminasorum bv. viciae 3841 journal February 2018
Genome-resolved metagenomics and metatranscriptomics of microbial communities in three meander-bound floodplain soils along the East River, Colorado.
  • Matheus Carnevali, Paula; Hobson, Chad; Geller-McGrath, David
  • Environmental System Science Data Infrastructure for a Virtual Ecosystem; Watershed Function SFA https://doi.org/10.15485/1631979
dataset January 2020
Metagenome-assembled genomes from Wind River Basin floodplain sediments Riverton, Wyoming site (August 2015) dataset January 2025
Metagenome-assembled genomes from Wind River Basin floodplain sediments Riverton, Wyoming site (June to October 2019) dataset January 2025
Human Alteration of the Global Nitrogen Cycle: Sources and Consequences journal August 1997
Hydrologic Connectivity to Streams Increases Nitrogen and Phosphorus Inputs and Cycling in Soils of Created and Natural Floodplain Wetlands journal July 2013
Evidence for Microbial Mediated NO3− Cycling Within Floodplain Sediments During Groundwater Fluctuations journal July 2019
Stability of Floodplain Subsurface Microbial Communities Through Seasonal Hydrological and Geochemical Cycles journal August 2020
Unraveling sources of cyanate in the marine environment: insights from cyanate distributions and production during the photochemical degradation of dissolved organic matter journal March 2024
Composted Cattle Manure Increases Microbial Activity and Soil Fertility More Than Composted Swine Manure in a Submerged Rice Paddy journal September 2017
Freshwater Sediment Microbial Communities Are Not Resilient to Disturbance From Agricultural Land Runoff journal October 2020
Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities journal August 2022
Genomic insight into strategy, interaction and evolution of nitrifiers in metabolizing key labile-dissolved organic nitrogen in different environmental niches journal December 2023
Allantoin: A Potential Compound for the Mitigation of Adverse Effects of Abiotic Stresses in Plants journal August 2023
Nutrient Retention in Ecologically Functional Floodplains: A Review journal October 2020
TheybcFGene ofEscherichia coliEncodes a Local Orphan Enzyme, Catabolic Carbamate Kinase journal November 2022
CONCOCT: Clustering cONtigs on COverage and ComposiTion preprint January 2013
CoverM: Read alignment statistics for metagenomics text January 2025
Anvi’o: an advanced analysis and visualization platform for ‘omics data journal January 2015
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies journal January 2019

Similar Records

Metagenome‐Assembled Genomes for Oligotrophic Nitrifiers From a Mountainous Gravelbed Floodplain
Journal Article · Tue Mar 18 00:00:00 EDT 2025 · Environmental Microbiology · OSTI ID:2575492

Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences
Journal Article · Tue Jan 30 23:00:00 EST 2024 · Nature Microbiology · OSTI ID:2287685