The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger

The ocean is an important global source of nitrous oxide (N2O), a greenhouse gas that contributes to stratospheric ozone destruction. Bacterial nitrification and denitrification are thought to be the primary sources of marine N2O, but the isotopic signatures of N2O produced by these processes are not consistent with the marine contribution to the global N2O budget. Based on enrichment cultures, we report that archaeal ammonia oxidation also produces N2O. Natural-abundance stable isotope measurements indicate that the produced N2O had bulk δ15N and δ18O values higher than observed for ammonia-oxidizing bacteria but similar to the δ15N and δ18O values attributed to the oceanic N2O source to the atmosphere. Our results suggest that ammonia-oxidizing archaea may be largely responsible for the oceanic N2O source.

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Nitrogen and Oxygen Isotope Effects of Ammonia Oxidation by Thermophilic Thaumarchaeota from a Geothermal Water Stream

Applied and Environmental Microbiology ◽

10.1128/aem.00250-16 ◽

2016 ◽

Vol 82 (15) ◽

pp. 4492-4504 ◽

Cited By ~ 14

Author(s):

Manabu Nishizawa ◽

Sanae Sakai ◽

Uta Konno ◽

Nozomi Nakahara ◽

Yoshihiro Takaki ◽

...

Keyword(s):

Oxygen Isotope ◽

Ammonia Oxidation ◽

Isotope Effects ◽

Isotope Ratios ◽

Oxidation Activity ◽

Content Type ◽

Ammonia Oxidizing Archaea ◽

Nitrogen Pools ◽

Archaeal Ammonia Oxidation

ABSTRACTAmmonia oxidation regulates the balance of reduced and oxidized nitrogen pools in nature. Although ammonia-oxidizing archaea have been recently recognized to often outnumber ammonia-oxidizing bacteria in various environments, the contribution of ammonia-oxidizing archaea is still uncertain due to difficulties in thein situquantification of ammonia oxidation activity. Nitrogen and oxygen isotope ratios of nitrite (δ15NNO2−and δ18ONO2−, respectively) are geochemical tracers for evaluating the sources and thein siturate of nitrite turnover determined from the activities of nitrification and denitrification; however, the isotope ratios of nitrite from archaeal ammonia oxidation have been characterized only for a few marine species. We first report the isotope effects of ammonia oxidation at 70°C by thermophilicThaumarchaeotapopulations composed almost entirely of “CandidatusNitrosocaldus.” The nitrogen isotope effect of ammonia oxidation varied with ambient pH (25‰ to 32‰) and strongly suggests the oxidation of ammonia, not ammonium. The δ18O value of nitrite produced from ammonia oxidation varied with the δ18O value of water in the medium but was lower than the isotopic equilibrium value in water. Because experiments have shown that the half-life of abiotic oxygen isotope exchange between nitrite and water is longer than 33 h at 70°C and pH ≥6.6, the rate of ammonia oxidation by thermophilicThaumarchaeotacould be estimated using δ18ONO2−in geothermal environments, where the biological nitrite turnover is likely faster than 33 h. This study extended the range of application of nitrite isotopes as a geochemical clock of the ammonia oxidation activity to high-temperature environments.IMPORTANCEBecause ammonia oxidation is generally the rate-limiting step in nitrification that regulates the balance of reduced and oxidized nitrogen pools in nature, it is important to understand the biological and environmental factors underlying the regulation of the rate of ammonia oxidation. The discovery of ammonia-oxidizing archaea (AOA) in marine and terrestrial environments has transformed the concept that ammonia oxidation is operated only by bacterial species, suggesting that AOA play a significant role in the global nitrogen cycle. However, the archaeal contribution to ammonia oxidation in the global biosphere is not yet completely understood. This study successfully identified key factors controlling nitrogen and oxygen isotopic ratios of nitrite produced from thermophilicThaumarchaeotaand elucidated the applicability and its limit of nitrite isotopes as a geochemical clock of ammonia oxidation rate in nature. Oxygen isotope analysis in this study also provided new biochemical information on archaeal ammonia oxidation.

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Nitric oxide scavengers differentially inhibit ammonia oxidation in ammonia-oxidizing archaea and bacteria

FEMS Microbiology Letters ◽

10.1093/femsle/fnw052 ◽

2016 ◽

Vol 363 (7) ◽

pp. fnw052 ◽

Cited By ~ 18

Author(s):

Laura A. Sauder ◽

Ashley A. Ross ◽

Josh D. Neufeld

Keyword(s):

Nitric Oxide ◽

Ammonia Oxidation ◽

Ammonia Oxidizing Archaea

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Oxygen production by an ammonia-oxidizing archaeon

10.1101/2021.04.01.436977 ◽

2021 ◽

Author(s):

Beate Kraft ◽

Nico Jehmlich ◽

Morten Larsen ◽

Laura Bristow ◽

Martin Koenneke ◽

...

Keyword(s):

Nitric Oxide ◽

Energy Metabolism ◽

Ammonia Oxidation ◽

Oxygen Production ◽

Ammonia Oxidizing Archaea ◽

Surrounding Environment ◽

Incubation Experiments ◽

Key Players ◽

Intermediate Part ◽

Nanomolar Range

Ammonia-oxidizing archaea (AOA) are one of the most abundant groups of microbes in the world's oceans and are key players in the nitrogen cycle. Their energy metabolism, the oxidation of ammonia to nitrite, requires oxygen. Nevertheless, AOA are abundant in environments where oxygen is undetectable. In incubation experiments, where oxygen concentrations were resolved to the nanomolar range, we show that Nitrosopumilus maritimus produces oxygen (O2) and dinitrogen (N2). The pathway is not completely resolved, but it has nitric oxide as a key intermediate. Part of the oxygen produced is directly used for ammonia oxidation, while some accumulates in the surrounding environment. N. maritimus joins a small handful of organisms known to produce oxygen in the dark, and based on this ability, we re-evaluate their role in oxygen-depleted marine environments.

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Soil ammonia-oxidizing archaea in a paddy field with different irrigation and fertilization managements

Scientific Reports ◽

10.1038/s41598-021-93898-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Limin Wang ◽

Dongfeng Huang

Keyword(s):

Ammonia Oxidation ◽

Chemical Properties ◽

Paddy Soils ◽

Soil Nitrification ◽

Treated Soil ◽

Ammonia Oxidizing Archaea ◽

Rice Yields ◽

Traditional Irrigation ◽

Almost All ◽

And Function

AbstractBecause ammonia-oxidizing archaea (AOA) are ubiquitous and highly abundant in almost all terrestrial soils, they play an important role in soil nitrification. However, the changes in the structure and function of AOA communities and their edaphic drivers in paddy soils under different fertilization and irrigation regimes remain unclear. In this study, we investigated AOA abundance, diversity and activity in acid paddy soils by a field experiment. Results indicated that the highest potential ammonia oxidation (PAO) (0.011 μg NO 2 - –N g-1 d.w.day-1) was found in T2 (optimal irrigation and fertilization)—treated soils, whereas the lowest PAO (0.004 μg NO 2 - –N g-1 d.w.day-1) in T0 (traditional irrigation)- treated soils. Compared with the T0—treated soil, the T2 treatment significantly (P < 0.05) increased AOA abundances. Furthermore, the abundance of AOA was significantly (P < 0.01) positively correlated with pH, soil organic carbon (SOC), and PAO. Meanwhile, pH and SOC content were significantly (P < 0.05) higher in the T2—treated soil than those in the T1 (traditional irrigation and fertilization)- treated soil. In addition, these two edaphic factors further influenced the AOA community composition. The AOA phylum Crenarchaeota was mainly found in the T2—treated soils. Phylogenetic analysis revealed that most of the identified OTUs of AOA were mainly affiliated with Crenarchaeota. Furthermore, the T2 treatment had higher rice yield than the T0 and T1 treatments. Together, our findings confirm that T2 might ameliorate soil chemical properties, regulate the AOA community structure, increase the AOA abundance, enhance PAO and consequently maintain rice yields in the present study.

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Measurements of nitrite production in and around the primary nitrite maximum in the central California Current

Biogeosciences ◽

10.5194/bg-10-7395-2013 ◽

2013 ◽

Vol 10 (11) ◽

pp. 7395-7410 ◽

Cited By ~ 47

Author(s):

A. E. Santoro ◽

C. M. Sakamoto ◽

J. M. Smith ◽

J. N. Plant ◽

A. L. Gehman ◽

...

Keyword(s):

Ammonia Oxidation ◽

Heterotrophic Bacteria ◽

California Current ◽

Euphotic Zone ◽

Ammonia Oxidizing Bacteria ◽

Central California ◽

Oxidation Rates ◽

Ammonia Oxidizing Archaea ◽

Nitrite Production ◽

Nh3 Oxidation

Abstract. Nitrite (NO2−) is a substrate for both oxidative and reductive microbial metabolism. NO2− accumulates at the base of the euphotic zone in oxygenated, stratified open-ocean water columns, forming a feature known as the primary nitrite maximum (PNM). Potential pathways of NO2− production include the oxidation of ammonia (NH3) by ammonia-oxidizing bacteria and archaea as well as assimilatory nitrate (NO3−) reduction by phytoplankton and heterotrophic bacteria. Measurements of NH3 oxidation and NO3− reduction to NO2− were conducted at two stations in the central California Current in the eastern North Pacific to determine the relative contributions of these processes to NO2− production in the PNM. Sensitive (< 10 nmol L−1), precise measurements of [NH4+] and [NO2−] indicated a persistent NH4+ maximum overlying the PNM at every station, with concentrations as high as 1.5 μmol L−1. Within and just below the PNM, NH3 oxidation was the dominant NO2− producing process, with rates of NH3 oxidation to NO2− of up to 31 nmol L−1 d−1, coinciding with high abundances of ammonia-oxidizing archaea. Though little NO2− production from NO3− was detected, potentially nitrate-reducing phytoplankton (photosynthetic picoeukaryotes, Synechococcus, and Prochlorococcus) were present at the depth of the PNM. Rates of NO2− production from NO3− were highest within the upper mixed layer (4.6 nmol L−1 d−1) but were either below detection limits or 10 times lower than NH3 oxidation rates around the PNM. One-dimensional modeling of water column NO2− production agreed with production determined from 15N bottle incubations within the PNM, but a modeled net biological sink for NO2− just below the PNM was not captured in the incubations. Residence time estimates of NO2− within the PNM ranged from 18 to 470 days at the mesotrophic station and was 40 days at the oligotrophic station. Our results suggest the PNM is a dynamic, rather than relict, feature with a source term dominated by ammonia oxidation.

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Transcriptional Response of the Archaeal Ammonia Oxidizer Nitrosopumilus maritimus to Low and Environmentally Relevant Ammonia Concentrations

Applied and Environmental Microbiology ◽

10.1128/aem.02028-13 ◽

2013 ◽

Vol 79 (22) ◽

pp. 6911-6916 ◽

Cited By ~ 28

Author(s):

Tatsunori Nakagawa ◽

David A. Stahl

Keyword(s):

Ammonia Oxidation ◽

Physiological State ◽

Transcriptional Response ◽

Ammonia Oxidizer ◽

Mrna Levels ◽

Marine Microorganisms ◽

Transcript Levels ◽

Content Type ◽

Ammonia Oxidizing Archaea ◽

Ammonia Transport

ABSTRACTThe ability of chemoautotrophic ammonia-oxidizing archaea to compete for ammonia among marine microorganisms at low ambient concentrations has been in part attributed to their extremely high affinity for ammonia, but as yet there is no mechanistic understanding of supporting metabolism. We examined transcription of selected genes for anabolic functions (CO2fixation, ammonia transport, and cell wall synthesis) and a central catabolic function (ammonia oxidation) in the thaumarchaeonNitrosopumilus maritimusSCM1 growing at two ammonia concentrations, as measured by combined ammonia and ammonium, one well above theKmfor ammonia oxidation (∼500 μM) and the other well below theKm(<10 nM). Transcript levels were generally immediately and differentially repressed when cells transitioned from ammonia-replete to ammonia-limiting conditions. Transcript levels for ammonia oxidation, CO2fixation, and one of the ammonia transport genes were approximately the same at high and low ammonia availability. Transcripts for all analyzed genes decreased with time in the complete absence of ammonia, but with various rates of decay. The new steady-state mRNA levels established are presumably more reflective of the natural physiological state of ammonia-oxidizing archaea and offer a reference for interpreting message abundance patterns in the natural environment.

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Archaea dominate oxic subseafloor communities over multimillion-year time scales

Science Advances ◽

10.1126/sciadv.aaw4108 ◽

2019 ◽

Vol 5 (6) ◽

pp. eaaw4108 ◽

Cited By ~ 24

Author(s):

Aurèle Vuillemin ◽

Scott D. Wankel ◽

Ömer K. Coskun ◽

Tobias Magritsch ◽

Sergio Vargas ◽

...

Keyword(s):

North Atlantic ◽

Organic Nitrogen ◽

Carbon Fixation ◽

Ammonia Oxidation ◽

North Atlantic Ocean ◽

Additional Energy ◽

Ammonia Oxidizing Archaea ◽

The North ◽

Metabolic Feature ◽

The North Atlantic

Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.

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Diversity of Ammonia-Oxidizing Archaea and Bacteria in the Sediments of a Hypernutrified Subtropical Estuary: Bahía del Tóbari, Mexico

Applied and Environmental Microbiology ◽

10.1128/aem.00946-06 ◽

2006 ◽

Vol 72 (12) ◽

pp. 7767-7777 ◽

Cited By ~ 181

Author(s):

J. Michael Beman ◽

Christopher A. Francis

Keyword(s):

Community Composition ◽

Ammonia Oxidation ◽

Pcr Primers ◽

Agricultural Runoff ◽

Detailed Examination ◽

Global Scale ◽

Estuarine Sediments ◽

Α Subunit ◽

Ammonia Oxidizing Archaea ◽

Subtropical Estuary

ABSTRACT Nitrification within estuarine sediments plays an important role in the nitrogen cycle, both at the global scale and in individual estuaries. Although bacteria were once thought to be solely responsible for catalyzing the first and rate-limiting step of this process, several recent studies have suggested that mesophilic Crenarchaeota are capable of performing ammonia oxidation. Here we examine the diversity (richness and community composition) of ammonia-oxidizing archaea (AOA) and bacteria (AOB) within sediments of Bahía del Tóbari, a hypernutrified estuary receiving substantial amounts of ammonium in agricultural runoff. Using PCR primers designed to specifically target the archaeal ammonia monooxygenase α-subunit (amoA) gene, we found AOA to be present at five sampling sites within this estuary and at two sampling time points (January and October 2004). In contrast, the bacterial amoA gene was PCR amplifiable from only 40% of samples. Bacterial amoA libraries were dominated by a few widely distributed Nitrosomonas-like sequence types, whereas AOA diversity showed significant variation in both richness and community composition. AOA communities nevertheless exhibited consistent spatial structuring, with two distinct end member assemblages recovered from the interior and the mouths of the estuary and a mixed assemblage from an intermediate site. These findings represent the first detailed examination of archaeal amoA diversity in estuarine sediments and demonstrate that diverse communities of Crenarchaeota capable of ammonia oxidation are present within estuaries, where they may be actively involved in nitrification.

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