Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea

Tolar, Bradley B.; Herrmann, Jonathan; Bargar, John R.; van den Bedem, Henry; Wakatsuki, Soichi; Francis, Christopher A.

doi:10.1111/1758-2229.12567

Title: Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea

Abstract

In this paper, knowledge of the molecular ecology and environmental determinants of ammonia-oxidizing organisms is critical to understanding and predicting the global nitrogen (N) and carbon cycles, but an incomplete biochemical picture hinders in vitro studies of N-cycling enzymes. Although an integrative structural and dynamic characterization at the atomic scale would advance our understanding of function tremendously, structural knowlede of key N-cycling enzymes from ecologically-relevant ammonia oxidizers is unfortunately extremely limited. Here, we discuss the challenges and opportunities for examining the ecology of ammonia-oxidizing organisms, particularly uncultivated Thaumarchaeota, though (meta)genome-driven structural biology of the enzymes ammonia monooxygenase (AMO) and nitrite reductase (NirK).

Authors:

Tolar, Bradley B. ^[1]; Herrmann, Jonathan ^[2]; Bargar, John R. ^[3]; van den Bedem, Henry ^[3]; Wakatsuki, Soichi ^[2]; Francis, Christopher A. ^[1]

Stanford Univ., Stanford, CA (United States)
Stanford Univ. School of Medicine, Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)

Publication Date:: Wed Jul 05 00:00:00 EDT 2017

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1366499

Grant/Contract Number:: AC02-76SF00515

Resource Type:: Accepted Manuscript

Journal Name:: Environmental Microbiology Reports

Additional Journal Information:: Journal Volume: 9; Journal Issue: 5; Journal ID: ISSN 1758-2229

Publisher:: Wiley-Blackwell

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES

Citation Formats


                    Tolar, Bradley B., Herrmann, Jonathan, Bargar, John R., van den Bedem, Henry, Wakatsuki, Soichi, and Francis, Christopher A. Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea.  United States: N. p., 2017. 
Web.  doi:10.1111/1758-2229.12567.

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                    Tolar, Bradley B., Herrmann, Jonathan, Bargar, John R., van den Bedem, Henry, Wakatsuki, Soichi, & Francis, Christopher A. Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea.  United States.  https://doi.org/10.1111/1758-2229.12567

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                    Tolar, Bradley B., Herrmann, Jonathan, Bargar, John R., van den Bedem, Henry, Wakatsuki, Soichi, and Francis, Christopher A. Wed .  
"Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea".  United States.  https://doi.org/10.1111/1758-2229.12567.  https://www.osti.gov/servlets/purl/1366499.

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@article{osti_1366499,

  title        = {Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea},

  author       = {Tolar, Bradley B. and Herrmann, Jonathan and Bargar, John R. and van den Bedem, Henry and Wakatsuki, Soichi and Francis, Christopher A.},

  abstractNote = {In this paper, knowledge of the molecular ecology and environmental determinants of ammonia-oxidizing organisms is critical to understanding and predicting the global nitrogen (N) and carbon cycles, but an incomplete biochemical picture hinders in vitro studies of N-cycling enzymes. Although an integrative structural and dynamic characterization at the atomic scale would advance our understanding of function tremendously, structural knowlede of key N-cycling enzymes from ecologically-relevant ammonia oxidizers is unfortunately extremely limited. Here, we discuss the challenges and opportunities for examining the ecology of ammonia-oxidizing organisms, particularly uncultivated Thaumarchaeota, though (meta)genome-driven structural biology of the enzymes ammonia monooxygenase (AMO) and nitrite reductase (NirK).},

  doi          = {10.1111/1758-2229.12567},

  journal      = {Environmental Microbiology Reports},

  number       = 5,

  volume       = 9,

  place        = {United States},

  year         = {Wed Jul 05 00:00:00 EDT 2017},

  month        = {Wed Jul 05 00:00:00 EDT 2017}

}

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Works referenced in this record:

Metabolism of Inorganic N Compounds by Ammonia-Oxidizing Bacteria
journal, January 2003

Arp, Daniel J.; Stein, Lisa Y.
Critical Reviews in Biochemistry and Molecular Biology, Vol. 38, Issue 6
DOI: 10.1080/10409230390267446

Enzymatic Mechanism of Copper-Containing Nitrite Reductase
journal, January 2015

Li, Yan; Hodak, Miroslav; Bernholc, J.
Biochemistry, Vol. 54, Issue 5
DOI: 10.1021/bi5007767

The archaeal cell envelope
journal, May 2011

Albers, Sonja-Verena; Meyer, Benjamin H.
Nature Reviews Microbiology, Vol. 9, Issue 6
DOI: 10.1038/nrmicro2576

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean
journal, December 2010

Shi, Yanmei; Tyson, Gene W.; Eppley, John M.
The ISME Journal, Vol. 5, Issue 6
DOI: 10.1038/ismej.2010.189

Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean
journal, September 2005

Francis, C. A.; Roberts, K. J.; Beman, J. M.
Proceedings of the National Academy of Sciences, Vol. 102, Issue 41, p. 14683-14688
DOI: 10.1073/pnas.0506625102

Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea
journal, December 2012

Vajrala, N.; Martens-Habbena, W.; Sayavedra-Soto, L. A.
Proceedings of the National Academy of Sciences, Vol. 110, Issue 3
DOI: 10.1073/pnas.1214272110

Integrative, dynamic structural biology at atomic resolution—it's about time
journal, March 2015

van den Bedem, Henry; Fraser, James S.
Nature Methods, Vol. 12, Issue 4
DOI: 10.1038/nmeth.3324

Suicidal inactivation and labelling of ammonia mono-oxygenase by acetylene
journal, May 1985

Hyman, M. R.; Wood, P. M.
Biochemical Journal, Vol. 227, Issue 3, p. 719-725
DOI: 10.1042/bj2270719

A simple method for displaying the hydropathic character of a protein
journal, May 1982

Kyte, Jack; Doolittle, Russell F.
Journal of Molecular Biology, Vol. 157, Issue 1, p. 105-132
DOI: 10.1016/0022-2836(82)90515-0

Environmental Genome Shotgun Sequencing of the Sargasso Sea
journal, April 2004

Venter, J. C.
Science, Vol. 304, Issue 5667
DOI: 10.1126/science.1093857

Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily: Structure of an Archaeal amoB Domain
journal, March 2014

Lawton, Thomas J.; Ham, Jungwha; Sun, Tianlin
Proteins: Structure, Function, and Bioinformatics, Vol. 82, Issue 9
DOI: 10.1002/prot.24535

Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats
journal, May 2012

Mosier, Annika C.; Lund, Marie B.; Francis, Christopher A.
Microbial Ecology, Vol. 64, Issue 4
DOI: 10.1007/s00248-012-0075-1

Environmental Calcium Controls Alternate Physical States of the Caulobacter Surface Layer
journal, May 2017

Herrmann, Jonathan; Jabbarpour, Fatemeh; Bargar, Paul G.
Biophysical Journal, Vol. 112, Issue 9
DOI: 10.1016/j.bpj.2017.04.003

The characterization of amino acid sequences in proteins by statistical methods
journal, November 1968

Zimmerman, J. M.; Eliezer, Naomi; Simha, R.
Journal of Theoretical Biology, Vol. 21, Issue 2
DOI: 10.1016/0022-5193(68)90069-6

Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea
journal, May 2012

Lund, Marie B.; Smith, Jason M.; Francis, Christopher A.
The ISME Journal, Vol. 6, Issue 10
DOI: 10.1038/ismej.2012.40

Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean
journal, January 2015

Santoro, Alyson E.; Dupont, Christopher L.; Richter, R. Alex
Proceedings of the National Academy of Sciences, Vol. 112, Issue 4
DOI: 10.1073/pnas.1416223112

Archaeal amo A gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean : Biogeography of archaeal ammonia oxidizers
journal, June 2012

Sintes, Eva; Bergauer, Kristin; De Corte, Daniele
Environmental Microbiology, Vol. 15, Issue 5
DOI: 10.1111/j.1462-2920.2012.02801.x

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
Nature Protocols, Vol. 10, Issue 6
DOI: 10.1038/nprot.2015.053

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation
journal, May 2014

Konneke, M.; Schubert, D. M.; Brown, P. C.
Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
DOI: 10.1073/pnas.1402028111

Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum
journal, November 2006

Hallam, S. J.; Konstantinidis, K. T.; Putnam, N.
Proceedings of the National Academy of Sciences, Vol. 103, Issue 48
DOI: 10.1073/pnas.0608549103

Isolation of an autotrophic ammonia-oxidizing marine archaeon
journal, September 2005

Könneke, Martin; Bernhard, Anne E.; de la Torre, José R.
Nature, Vol. 437, Issue 7058
DOI: 10.1038/nature03911

A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters
journal, April 2012

Williams, Timothy J.; Long, Emilie; Evans, Flavia
The ISME Journal, Vol. 6, Issue 10
DOI: 10.1038/ismej.2012.28

Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context: Nitrite reductase of soil archaea
journal, February 2010

Bartossek, Rita; Nicol, Graeme W.; Lanzen, Anders
Environmental Microbiology, Vol. 12, Issue 4
DOI: 10.1111/j.1462-2920.2010.02153.x

Enzymatic Oxidation of Methane
journal, March 2015

Sirajuddin, Sarah; Rosenzweig, Amy C.
Biochemistry, Vol. 54, Issue 14
DOI: 10.1021/acs.biochem.5b00198

Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage
journal, November 2010

Hollibaugh, James T.; Gifford, Scott; Sharma, Shalabh
The ISME Journal, Vol. 5, Issue 5
DOI: 10.1038/ismej.2010.172

Metagenomic Analysis of Ammonia-Oxidizing Archaea Affiliated with the Soil Group
journal, January 2012

Bartossek, Rita; Spang, Anja; Weidler, Gerhard
Frontiers in Microbiology, Vol. 3
DOI: 10.3389/fmicb.2012.00208

Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea
journal, April 2010

Walker, C. B.; de la Torre, J. R.; Klotz, M. G.
Proceedings of the National Academy of Sciences, Vol. 107, Issue 19
DOI: 10.1073/pnas.0913533107

Serial crystallography captures enzyme catalysis in copper nitrite reductase at atomic resolution from one crystal
journal, June 2016

Horrell, Sam; Antonyuk, Svetlana V.; Eady, Robert R.
IUCrJ, Vol. 3, Issue 4
DOI: 10.1107/S205225251600823X

Crystal Structure and Characterization of Particulate Methane Monooxygenase from Methylocystis species Strain M
journal, November 2011

Smith, Stephen M.; Rawat, Swati; Telser, Joshua
Biochemistry, Vol. 50, Issue 47
DOI: 10.1021/bi200801z

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota
journal, February 2016

Kozlowski, Jessica A.; Stieglmeier, Michaela; Schleper, Christa
The ISME Journal, Vol. 10, Issue 8
DOI: 10.1038/ismej.2016.2

Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling: Role of mesophilic crenarchaeota in nitrogen cycling
journal, September 2005

Treusch, Alexander H.; Leininger, Sven; Kletzin, Arnulf
Environmental Microbiology, Vol. 7, Issue 12
DOI: 10.1111/j.1462-2920.2005.00906.x

Responses of the terrestrial ammonia-oxidizing archaeon Ca . Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors
journal, May 2013

Shen, Tianlin; Stieglmeier, Michaela; Dai, Jiulan
FEMS Microbiology Letters, Vol. 344, Issue 2
DOI: 10.1111/1574-6968.12164

The Divergent AmoC3 Subunit of Ammonia Monooxygenase Functions as Part of a Stress Response System in Nitrosomonas europaea
journal, April 2012

Berube, P. M.; Stahl, D. A.
Journal of Bacteriology, Vol. 194, Issue 13
DOI: 10.1128/JB.00133-12

Oxidation of methane by a biological dicopper centre
journal, April 2010

Balasubramanian, Ramakrishnan; Smith, Stephen M.; Rawat, Swati
Nature, Vol. 465, Issue 7294
DOI: 10.1038/nature08992

Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012

Stahl, David A.; de la Torre, José R.
Annual Review of Microbiology, Vol. 66, Issue 1
DOI: 10.1146/annurev-micro-092611-150128

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers
journal, November 2016

Kerou, Melina; Offre, Pierre; Valledor, Luis
Proceedings of the National Academy of Sciences, Vol. 113, Issue 49
DOI: 10.1073/pnas.1601212113

Global Biodiversity of Aquatic Ammonia-Oxidizing Archaea is Partitioned by Habitat
journal, January 2012

Biller, Steven J.; Mosier, Annika C.; Wells, George F.
Frontiers in Microbiology, Vol. 3
DOI: 10.3389/fmicb.2012.00252

Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters
journal, February 2014

Smith, Jason M.; Casciotti, Karen L.; Chavez, Francisco P.
The ISME Journal, Vol. 8, Issue 8
DOI: 10.1038/ismej.2014.11

Electron paramagnetic studies of the copper and iron containing soluble ammonia monooxygenase from Nitrosomonas europaea
journal, March 2010

Gilch, Stefan; Meyer, Ortwin; Schmidt, Ingo
BioMetals, Vol. 23, Issue 4
DOI: 10.1007/s10534-010-9308-2

Works referencing / citing this record:

Depth distributions of nitrite reductase ( nirK ) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay
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Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies
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Global Change Biology, Vol. 26, Issue 1
DOI: 10.1111/gcb.14877

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Title: Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea

Abstract

Citation Formats

Metabolism of Inorganic N Compounds by Ammonia-Oxidizing Bacteria journal, January 2003

Enzymatic Mechanism of Copper-Containing Nitrite Reductase journal, January 2015

The archaeal cell envelope journal, May 2011

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean journal, December 2010

Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean journal, September 2005

Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea journal, December 2012

Integrative, dynamic structural biology at atomic resolution—it's about time journal, March 2015

Suicidal inactivation and labelling of ammonia mono-oxygenase by acetylene journal, May 1985

A simple method for displaying the hydropathic character of a protein journal, May 1982

Environmental Genome Shotgun Sequencing of the Sargasso Sea journal, April 2004

Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily: Structure of an Archaeal amoB Domain journal, March 2014

Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats journal, May 2012

Environmental Calcium Controls Alternate Physical States of the Caulobacter Surface Layer journal, May 2017

The characterization of amino acid sequences in proteins by statistical methods journal, November 1968

Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea journal, May 2012

Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean journal, January 2015

Archaeal amo A gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean : Biogeography of archaeal ammonia oxidizers journal, June 2012

The Phyre2 web portal for protein modeling, prediction and analysis journal, May 2015

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation journal, May 2014

Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum journal, November 2006

Isolation of an autotrophic ammonia-oxidizing marine archaeon journal, September 2005

A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters journal, April 2012

Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context: Nitrite reductase of soil archaea journal, February 2010

Enzymatic Oxidation of Methane journal, March 2015

Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage journal, November 2010

Metagenomic Analysis of Ammonia-Oxidizing Archaea Affiliated with the Soil Group journal, January 2012

Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea journal, April 2010

Serial crystallography captures enzyme catalysis in copper nitrite reductase at atomic resolution from one crystal journal, June 2016

Crystal Structure and Characterization of Particulate Methane Monooxygenase from Methylocystis species Strain M journal, November 2011

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota journal, February 2016

Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling: Role of mesophilic crenarchaeota in nitrogen cycling journal, September 2005

Responses of the terrestrial ammonia-oxidizing archaeon Ca . Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors journal, May 2013

The Divergent AmoC3 Subunit of Ammonia Monooxygenase Functions as Part of a Stress Response System in Nitrosomonas europaea journal, April 2012

Oxidation of methane by a biological dicopper centre journal, April 2010

Physiology and Diversity of Ammonia-Oxidizing Archaea journal, October 2012

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers journal, November 2016

Global Biodiversity of Aquatic Ammonia-Oxidizing Archaea is Partitioned by Habitat journal, January 2012

Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters journal, February 2014

Electron paramagnetic studies of the copper and iron containing soluble ammonia monooxygenase from Nitrosomonas europaea journal, March 2010

Depth distributions of nitrite reductase ( nirK ) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay journal, August 2019

Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies journal, November 2019

Metabolism of Inorganic N Compounds by Ammonia-Oxidizing Bacteria
journal, January 2003

Enzymatic Mechanism of Copper-Containing Nitrite Reductase
journal, January 2015

The archaeal cell envelope
journal, May 2011

Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean
journal, December 2010

Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean
journal, September 2005

Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea
journal, December 2012

Integrative, dynamic structural biology at atomic resolution—it's about time
journal, March 2015

Suicidal inactivation and labelling of ammonia mono-oxygenase by acetylene
journal, May 1985

A simple method for displaying the hydropathic character of a protein
journal, May 1982

Environmental Genome Shotgun Sequencing of the Sargasso Sea
journal, April 2004

Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily: Structure of an Archaeal amoB Domain
journal, March 2014

Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats
journal, May 2012

Environmental Calcium Controls Alternate Physical States of the Caulobacter Surface Layer
journal, May 2017

The characterization of amino acid sequences in proteins by statistical methods
journal, November 1968

Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea
journal, May 2012

Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean
journal, January 2015

Archaeal amo A gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean : Biogeography of archaeal ammonia oxidizers
journal, June 2012

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation
journal, May 2014

Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum
journal, November 2006

Isolation of an autotrophic ammonia-oxidizing marine archaeon
journal, September 2005

A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters
journal, April 2012

Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context: Nitrite reductase of soil archaea
journal, February 2010

Enzymatic Oxidation of Methane
journal, March 2015

Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage
journal, November 2010

Metagenomic Analysis of Ammonia-Oxidizing Archaea Affiliated with the Soil Group
journal, January 2012

Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea
journal, April 2010

Serial crystallography captures enzyme catalysis in copper nitrite reductase at atomic resolution from one crystal
journal, June 2016

Crystal Structure and Characterization of Particulate Methane Monooxygenase from Methylocystis species Strain M
journal, November 2011

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota
journal, February 2016

Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling: Role of mesophilic crenarchaeota in nitrogen cycling
journal, September 2005

Responses of the terrestrial ammonia-oxidizing archaeon Ca . Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors
journal, May 2013

The Divergent AmoC3 Subunit of Ammonia Monooxygenase Functions as Part of a Stress Response System in Nitrosomonas europaea
journal, April 2012

Oxidation of methane by a biological dicopper centre
journal, April 2010

Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers
journal, November 2016

Global Biodiversity of Aquatic Ammonia-Oxidizing Archaea is Partitioned by Habitat
journal, January 2012

Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters
journal, February 2014

Electron paramagnetic studies of the copper and iron containing soluble ammonia monooxygenase from Nitrosomonas europaea
journal, March 2010

Depth distributions of nitrite reductase ( nirK ) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay
journal, August 2019

Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies
journal, November 2019