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

Title: Metagenomic recovery of two distinct comammox Nitrospira from the terrestrial subsurface

Journal Article · · Environmental Microbiology

The recently discovered comammox process encompasses both nitrification steps, the aerobic oxidation of ammonia and nitrite, in a single organism. All known comammox bacteria are affiliated with Nitrospira sublineage II and can be grouped into two distinct clades, referred to as A and B, based on ammonia monooxygenase phylogeny. In this study, we report high-quality draft genomes of two novel comammox Nitrospira from the terrestrial subsurface, representing one clade A and one clade B comammox organism. The two metagenome-assembled genomes were compared with other representatives of Nitrospira sublineage II, including both canonical and comammox Nitrospira. Phylogenomic analyses confirmed the affiliation of the two novel Nitrospira with comammox clades A and B respectively. Based on phylogenetic distance and pairwise average nucleotide identity values, both comammox Nitrospira were classified as novel species. Genomic comparison revealed high conservation of key metabolic features in sublineage II Nitrospira, including respiratory complexes I-V and the machineries for nitrite oxidation and carbon fixation via the reductive tricarboxylic acid cycle. In addition, the presence of the enzymatic repertoire for formate and hydrogen oxidation in the Rifle clades A and B comammox genomes, respectively, suggest a broader distribution of these metabolic features than previously anticipated.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE
Grant/Contract Number:
AC02-05CH11231; AC02‐05CH11231; DE‐AC02‐05CH11231
OSTI ID:
1569086
Alternate ID(s):
OSTI ID: 1569087; OSTI ID: 1572063
Journal Information:
Environmental Microbiology, Vol. 21, Issue 10; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 52 works
Citation information provided by
Web of Science

References (118)

Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase journal July 2017
Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira journal March 2018
Ecological patterns, diversity and core taxa of microbial communities in groundwater-fed rapid gravity filters journal March 2016
UniProt: the universal protein knowledgebase journal November 2016
Cyanate as an energy source for nitrifiers journal July 2015
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
ATP Hydrolysis and Synthesis of a Rotary Motor V-ATPase from Thermus thermophilus journal May 2008
Enterococcus hirae vacuolar ATPase is expressed in response to pH as well as sodium journal July 1999
The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer journal January 2013
Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation journal August 2014
genoPlotR: comparative gene and genome visualization in R journal July 2010
UniRef: comprehensive and non-redundant UniProt reference clusters journal March 2007
Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil journal May 2014
The 1.3-A resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins journal November 2007
SignalP 4.0: discriminating signal peptides from transmembrane regions journal September 2011
Metalloenzyme nitrile hydratase: Structure, regulation, and application to biotechnology journal August 1998
Characterization of Hydrogenase II from the Hyperthermophilic Archaeon Pyrococcus furiosus and Assessment of Its Role in Sulfur Reduction journal April 2000
Freshwater Recirculating Aquaculture System Operations Drive Biofilter Bacterial Community Shifts around a Stable Nitrifying Consortium of Ammonia-Oxidizing Archaea and Comammox Nitrospira journal January 2017
Stress response of a marine ammonia-oxidizing archaeon informs physiological status of environmental populations journal October 2017
Metagenomic Evidence for the Presence of Comammox Nitrospira -Like Bacteria in a Drinking Water System journal November 2015
A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria journal July 2010
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities journal January 2015
Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition journal November 2018
Nitrile Hydratase and Amidase from Rhodococcus rhodochrous Hydrolyze Acrylic Fibers and Granular Polyacrylonitriles journal April 2000
In Situ Characterization of Nitrospira-Like Nitrite-Oxidizing Bacteria Active in Wastewater Treatment Plants journal November 2001
NADH:ferredoxin reductase and NAD-reducing hydrogenase activities in Hydrogenobacter thermophilus strain TK-6 journal June 1996
An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia journal July 2014
Functionally relevant diversity of closely related Nitrospira in activated sludge journal August 2014
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Author Correction: Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life journal December 2017
The SLC26 gene family of anion transporters and channels journal April 2013
Aquifer environment selects for microbial species cohorts in sediment and groundwater journal February 2015
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 1999
UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction journal February 2018
A Combined Transmembrane Topology and Signal Peptide Prediction Method journal May 2004
Variability of the transporter gene complement in ammonia-oxidizing archaea journal December 2014
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy journal May 2018
The AmiE aliphatic amidase and AmiF formamidase of Helicobacter pylori: natural evolution of two enzyme paralogues: Study of the two paralogous amidases of H. pylori journal May 2001
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions journal May 2008
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Prokka: rapid prokaryotic genome annotation journal March 2014
Genomic Analysis of Two Phylogenetically Distinct Nitrospira Species Reveals Their Genomic Plasticity and Functional Diversity journal January 2018
Complete nitrification by Nitrospira bacteria journal November 2015
Why is metabolic labour divided in nitrification? journal May 2006
Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira journal August 2015
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring: Moderately thermophilic Nitrospira-cultures from hot springs journal December 2010
Binning metagenomic contigs by coverage and composition journal September 2014
Connecting stalks in V-type ATPase journal September 1999
A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria journal September 2016
Complete nitrification by a single microorganism journal November 2015
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation journal November 2015
AmoA-Targeted Polymerase Chain Reaction Primers for the Specific Detection and Quantification of Comammox Nitrospira in the Environment journal August 2017
Fast gapped-read alignment with Bowtie 2 journal March 2012
Creating the CIPRES Science Gateway for inference of large phylogenetic trees conference November 2010
Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines journal December 2015
Basic local alignment search tool journal October 1990
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
SODa: An Mn/Fe superoxide dismutase prediction and design server journal January 2008
Complete nitrification: insights into the ecophysiology of comammox Nitrospira journal November 2018
Molecular aspects of bacterial pH sensing and homeostasis journal April 2011
Comammox in drinking water systems journal June 2017
Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization journal November 2017
Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. journal March 1996
A large-scale evaluation of algorithms to calculate average nucleotide identity journal February 2017
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Ubiquity and Diversity of Complete Ammonia Oxidizers (Comammox) journal October 2018
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment journal August 2013
Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle journal October 2017
Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle journal August 2017
Lysobacter telluris sp. nov., isolated from Korean rhizosphere soil journal September 2020
An SHR–SCR module specifies legume cortical cell fate to enable nodulation journal December 2020
UniProt: the Universal Protein knowledgebase journal January 2004
Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea journal February 2021
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies text January 2014
UniProt: the universal protein knowledgebase journal February 2018
Complete nitrification by a single microorganism audiovisual January 2021
Complete nitrification: insights into the ecophysiology of comammox Nitrospira journal November 2018
A large-scale evaluation of algorithms to calculate average nucleotide identity journal February 2017
UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction journal February 2018
A Combined Transmembrane Topology and Signal Peptide Prediction Method journal May 2004
The SLC26 gene family of anion transporters and channels journal April 2013
Why is metabolic labour divided in nitrification? journal May 2006
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
Comammox in drinking water systems journal June 2017
Connecting stalks in V-type ATPase journal September 1999
Functionally relevant diversity of closely related Nitrospira in activated sludge journal August 2014
Aquifer environment selects for microbial species cohorts in sediment and groundwater journal February 2015
Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines journal December 2015
Ecological patterns, diversity and core taxa of microbial communities in groundwater-fed rapid gravity filters journal March 2016
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
Cyanate as an energy source for nitrifiers journal July 2015
Complete nitrification by a single microorganism journal November 2015
Complete nitrification by Nitrospira bacteria journal November 2015
SignalP 4.0: discriminating signal peptides from transmembrane regions journal September 2011
Molecular aspects of bacterial pH sensing and homeostasis journal April 2011
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria journal July 2010
An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia journal July 2014
UniRef: comprehensive and non-redundant UniProt reference clusters journal March 2007
genoPlotR: comparative gene and genome visualization in R journal July 2010
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Prokka: rapid prokaryotic genome annotation journal March 2014
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 1999
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation journal November 2015
UniProt: the universal protein knowledgebase journal November 2016
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions journal May 2008
Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. journal March 1996
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
SODa: An Mn/Fe superoxide dismutase prediction and design server journal January 2008
Freshwater Recirculating Aquaculture System Operations Drive Biofilter Bacterial Community Shifts around a Stable Nitrifying Consortium of Ammonia-Oxidizing Archaea and Comammox Nitrospira journal January 2017
AmoA-Targeted Polymerase Chain Reaction Primers for the Specific Detection and Quantification of Comammox Nitrospira in the Environment journal August 2017
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies text January 2014
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities journal January 2015

Cited By (3)