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

Title: Depth distributions of nitrite reductase ( nirK ) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay

Journal Article · · Environmental Microbiology
 [1];  [1];  [2];  [3]; ORCiD logo [1]
  1. Department of Earth System Science Stanford University Stanford CA
  2. Monterey Bay Aquarium Research Institute Moss Landing CA, Marine Science Institute University of California Santa Barbara Santa Barbara CA
  3. Monterey Bay Aquarium Research Institute Moss Landing CA

Summary Ammonia‐oxidizing archaea (AOA) of the phylum Thaumarchaeota are key players in nutrient cycling, yet large gaps remain in our understanding of their ecology and metabolism. Despite multiple lines of evidence pointing to a central role for copper‐containing nitrite reductase (NirK) in AOA metabolism, the thaumarchaeal nirK gene is rarely studied in the environment. In this study, we examine the diversity of nirK in the marine pelagic environment, in light of previously described ecological patterns of pelagic thaumarchaeal populations. Phylogenetic analyses show that nirK better resolves diversification patterns of marine Thaumarchaeota , compared to the conventionally used marker gene amoA . Specifically, we demonstrate that the three major phylogenetic clusters of marine nirK correspond to the three ‘ecotype’ populations of pelagic Thaumarchaeota . In this context, we further examine the relative distributions of the three variant groups in metagenomes and metatranscriptomes representing two depth profiles in coastal Monterey Bay. Our results reveal that nirK effectively tracks the dynamics of thaumarchaeal ecotype populations, particularly finer‐scale diversification patterns within major lineages. We also find evidence for multiple copies of nirK per genome in a fraction of thaumarchaeal cells in the water column, which must be taken into account when using it as a molecular marker.

Sponsoring Organization:
USDOE
OSTI ID:
1549194
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 11 Vol. 21; ISSN 1462-2912
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (58)

Factors influencing nitrification rates and the abundance and transcriptional activity of ammonia-oxidizing microorganisms in the dark northeast Pacific Ocean: Nitrification and AOA in the Dark Ocean journal December 2015
Thaumarchaeal ecotype distributions across the equatorial Pacific Ocean and their potential roles in nitrification and sinking flux attenuation: Thaumarchaea in the equatorial Pacific journal April 2017
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices journal June 2016
Archaeal dominance in the mesopelagic zone of the Pacific Ocean journal January 2001
Erratum: Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California journal April 2008
Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage journal November 2010
Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean journal December 2010
A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters journal April 2012
Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea journal May 2012
Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone journal September 2013
Single-cell genomics shedding light on marine Thaumarchaeota diversification journal November 2013
Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters journal February 2014
Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production journal August 2014
Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota journal July 2015
Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation journal November 2015
Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota journal February 2016
Contribution of ammonia oxidation to chemoautotrophy in Antarctic coastal waters journal May 2016
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
Isolation of an autotrophic ammonia-oxidizing marine archaeon journal September 2005
Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column journal January 2019
Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes journal April 2018
Renewing Felsenstein’s phylogenetic bootstrap in the era of big data journal April 2018
Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean journal September 2005
Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum journal November 2006
Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea journal April 2010
Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers journal November 2016
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
BFC: correcting Illumina sequencing errors journal May 2015
Utilization of urea and cyanate in waters overlying and within the eastern tropical north Pacific oxygen deficient zone journal July 2018
Pangenome Evidence for Extensive Interdomain Horizontal Transfer Affecting Lineage Core and Shell Genes in Uncultured Planktonic Thaumarchaeota and Euryarchaeota journal June 2014
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform journal July 2002
IMG: the integrated microbial genomes database and comparative analysis system journal December 2011
GenBank journal November 2015
IMG/M: integrated genome and metagenome comparative data analysis system journal October 2016
Gene duplication as a mechanism of genomic adaptation to a changing environment journal October 2012
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
The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger: Marine AOA produce NO and are inhibited by NO scavenger journal January 2015
Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems: Genome and epigenome of a new marine thaumarchaeon journal May 2017
Patterns of thaumarchaeal gene expression in culture and diverse marine environments journal April 2018
Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea: Structural biology insights into key AOA enzymes journal July 2017
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data journal September 2016
Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context: Nitrite reductase of soil archaea journal February 2010
Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current: Nitrification in the central California Current journal March 2010
Archaeal amo A gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean : Biogeography of archaeal ammonia oxidizers journal June 2012
Differential photoinhibition of bacterial and archaeal ammonia oxidation journal December 2011
Isotopic Signature of N2O Produced by Marine Ammonia-Oxidizing Archaea journal July 2011
Physiology and Diversity of Ammonia-Oxidizing Archaea journal October 2012
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree journal October 2010
Nitric Oxide Production from Nitrite Reduction and Hydroxylamine Oxidation by Copper-containing Dissimilatory Nitrite Reductase (NirK) from the Aerobic Ammonia-oxidizing Archaeon, Nitrososphaera viennensis journal January 2018
Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota journal March 2006
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Geographic Distribution of Archaeal Ammonia Oxidizing Ecotypes in the Atlantic Ocean journal February 2016
Niche Partitioning of the N Cycling Microbial Community of an Offshore Oxygen Deficient Zone journal December 2017
Spatiotemporal Dynamics of Ammonia-Oxidizing Thaumarchaeota in Distinct Arctic Water Masses journal January 2018
Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome journal January 2018
Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland journal February 2018