Isotopic Signature of N2O Produced by Marine Ammonia-Oxidizing Archaea

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.

Download Full-text

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.

Download Full-text

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.

Download Full-text

Ecophysiological Characterization of Ammonia-Oxidizing Archaea and Bacteria from Freshwater

Applied and Environmental Microbiology ◽

10.1128/aem.00432-12 ◽

2012 ◽

Vol 78 (16) ◽

pp. 5773-5780 ◽

Cited By ~ 113

Author(s):

Elizabeth French ◽

Jessica A. Kozlowski ◽

Maitreyee Mukherjee ◽

George Bullerjahn ◽

Annette Bollmann

Keyword(s):

Growth Rates ◽

Ammonia Oxidation ◽

Light Exposure ◽

Enrichment Culture ◽

Ammonia Oxidizing Bacteria ◽

Content Type ◽

Ammonia Oxidizing Archaea ◽

Group I ◽

Nitrosomonas Oligotropha

ABSTRACTAerobic biological ammonia oxidation is carried out by two groups of microorganisms, ammonia-oxidizing bacteria (AOB) and the recently discovered ammonia-oxidizing archaea (AOA). Here we present a study using cultivation-based methods to investigate the differences in growth of three AOA cultures and one AOB culture enriched from freshwater environments. The strain in the enriched AOA culture belong to thaumarchaeal group I.1a, with the strain in one enrichment culture having the highest identity with “CandidatusNitrosoarchaeum koreensis” and the strains in the other two representing a new genus of AOA. The AOB strain in the enrichment culture was also obtained from freshwater and had the highest identity to AOB from theNitrosomonas oligotrophagroup (Nitrosomonascluster 6a). We investigated the influence of ammonium, oxygen, pH, and light on the growth of AOA and AOB. The growth rates of the AOB increased with increasing ammonium concentrations, while the growth rates of the AOA decreased slightly. Increasing oxygen concentrations led to an increase in the growth rate of the AOB, while the growth rates of AOA were almost oxygen insensitive. Light exposure (white and blue wavelengths) inhibited the growth of AOA completely, and the AOA did not recover when transferred to the dark. AOB were also inhibited by blue light; however, growth recovered immediately after transfer to the dark. Our results show that the tested AOB have a competitive advantage over the tested AOA under most conditions investigated. Further experiments will elucidate the niches of AOA and AOB in more detail.

Download Full-text

Microbial N Transformations and N2O Emission after Simulated Grassland Cultivation: Effects of the Nitrification Inhibitor 3,4-Dimethylpyrazole Phosphate (DMPP)

Applied and Environmental Microbiology ◽

10.1128/aem.02019-16 ◽

2016 ◽

Vol 83 (1) ◽

Cited By ~ 23

Author(s):

Yun-Feng Duan ◽

Xian-Wang Kong ◽

Andreas Schramm ◽

Rodrigo Labouriau ◽

Jørgen Eriksen ◽

...

Keyword(s):

Adverse Effects ◽

Ammonia Oxidation ◽

Nitrification Inhibitor ◽

Transcript Abundance ◽

N Leaching ◽

Ammonia Oxidizing Bacteria ◽

N Losses ◽

Mineral N ◽

N Transformations ◽

Ammonia Oxidizing Archaea

ABSTRACT Grassland cultivation can mobilize large pools of N in the soil, with the potential for N leaching and N2O emissions. Spraying with the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) before cultivation was simulated by use of soil columns in which the residue distribution corresponded to plowing or rotovation to study the effects of soil-residue contact on N transformations. DMPP was sprayed on aboveground parts of ryegrass and white clover plants before incorporation. During a 42-day incubation, soil mineral N dynamics, potential ammonia oxidation (PAO), denitrifying enzyme activity (DEA), nitrifier and denitrifier populations, and N2O emissions were investigated. The soil NO3 − pool was enriched with 15N to trace sources of N2O. Ammonium was rapidly released from decomposing residues, and PAO was stimulated in soil near residues. DMPP effectively reduced NH4 + transformation irrespective of residue distribution. Ammonia-oxidizing archaea (AOA) and bacteria (AOB) were both present, but only the AOB amoA transcript abundance correlated with PAO. DMPP inhibited the transcription of AOB amoA genes. Denitrifier genes and transcripts (nirK, nirS, and clades I and II of nosZ) were recovered, and a correlation was found between nirS mRNA and DEA. DMPP showed no adverse effects on the abundance or activity of denitrifiers. The 15N enrichment of N2O showed that denitrification was responsible for 80 to 90% of emissions. With support from a control experiment without NO3 − amendment, it was concluded that DMPP will generally reduce the potential for leaching of residue-derived N, whereas the effect of DMPP on N2O emissions will be significant only when soil NO3 − availability is limiting. IMPORTANCE Residue incorporation following grassland cultivation can lead to mobilization of large pools of N and potentially to significant N losses via leaching and N2O emissions. This study proposed a mitigation strategy of applying 3,4-dimethylpyrazole phosphate (DMPP) prior to grassland cultivation and investigated its efficacy in a laboratory incubation study. DMPP inhibited the growth and activity of ammonia-oxidizing bacteria but had no adverse effects on ammonia-oxidizing archaea and denitrifiers. DMPP can effectively reduce the potential for leaching of NO3 − derived from residue decomposition, while the effect on reducing N2O emissions will be significant only when soil NO3 − availability is limiting. Our findings provide insight into how DMPP affects soil nitrifier and denitrifier populations and have direct implications for improving N use efficiency and reducing environmental impacts during grassland cultivation.

Download Full-text

The Response of Estuarine Ammonia-Oxidizing Communities to Constant and Fluctuating Salinity Regimes

Frontiers in Microbiology ◽

10.3389/fmicb.2020.574815 ◽

2020 ◽

Vol 11 ◽

Author(s):

João Pereira Santos ◽

António G. G. Sousa ◽

Hugo Ribeiro ◽

Catarina Magalhães

Keyword(s):

Ammonia Oxidation ◽

Estuarine Sediments ◽

Ammonia Oxidizer ◽

Rrna Gene ◽

Ammonia Oxidizing Bacteria ◽

Salinity Regime ◽

Salinity Fluctuation ◽

Ammonia Oxidizing Archaea ◽

Negative Effect ◽

The Impact

Aerobic nitrification is a fundamental nitrogen biogeochemical process that links the oxidation of ammonia to the removal of fixed nitrogen in eutrophicated water bodies. However, in estuarine environments there is an enormous variability of water physicochemical parameters that can affect the ammonia oxidation biological process. For instance, it is known that salinity can affect nitrification performance, yet there is still a lack of information on the ammonia-oxidizing communities behavior facing daily salinity fluctuations. In this work, laboratory experiments using upstream and downstream estuarine sediments were performed to address this missing gap by comparing the effect of daily salinity fluctuations with constant salinity on the activity and diversity of ammonia-oxidizing microorganisms (AOM). Activity and composition of AOM were assessed, respectively by using nitrogen stable isotope technique and 16S rRNA gene metabarcoding analysis. Nitrification activity was negatively affected by daily salinity fluctuations in upstream sediments while no effect was observed in downstream sediments. Constant salinity regime showed clearly higher rates of nitrification in upstream sediments while a similar nitrification performance between the two salinity regimes was registered in the downstream sediments. Results also indicated that daily salinity fluctuation regime had a negative effect on both ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) community’s diversity. Phylogenetically, the estuarine downstream AOM were dominated by AOA (0.92–2.09%) followed by NOB (0.99–2%), and then AOB (0.2–0.32%); whereas NOB dominated estuarine upstream sediment samples (1.4–9.5%), followed by AOA (0.27–0.51%) and AOB (0.01–0.23%). Analysis of variance identified the spatial difference between samples (downstream and upstream) as the main drivers of AOA and AOB diversity. Our study indicates that benthic AOM inhabiting different estuarine sites presented distinct plasticity toward the salinity regimes tested. These findings help to improve our understanding in the dynamics of the nitrogen cycle of estuarine systems by showing the resilience and consequently the impact of different salinity regimes on the diversity and activity of ammonia oxidizer communities.

Download Full-text

Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities

10.1101/2021.03.02.433310 ◽

2021 ◽

Author(s):

Man-Young Jung ◽

Christopher J. Sedlacek ◽

K. Dimitri Kits ◽

Anna J. Mueller ◽

Sung-Keun Rhee ◽

...

Keyword(s):

Ammonia Oxidation ◽

Oxidation Kinetic ◽

Ammonia Oxidizer ◽

Substrate Affinity ◽

Kinetic Properties ◽

Ammonia Oxidizing Bacteria ◽

Ammonia Oxidizers ◽

Kinetic Measurements ◽

Ammonia Oxidizing Archaea ◽

Wide Range

AbstractNitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co- occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest substrate affinity of any characterized AOA, which are similar to previously determined affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values strongly supports the hypothesis that – like for AOB – ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.

Download Full-text

Ammonia-oxidizing Archaea (AOA) are Winners to Survive in Oxygen-limited Habitat Compared to Ammonia-oxidizing Bacteria (AOB)

10.21203/rs.3.rs-201180/v1 ◽

2021 ◽

Author(s):

Peigang Dai ◽

Wenjing Song ◽

Zhao Che ◽

Lili Zhang ◽

Zhaorong Dong

Keyword(s):

Intertidal Zone ◽

High Throughput Sequencing ◽

Ammonia Oxidation ◽

Illumina Miseq ◽

Gene Copy ◽

Ammonia Oxidizing Bacteria ◽

Niche Specialization ◽

Ammonia Oxidizing Archaea ◽

Copy Numbers ◽

Oxidation Reduction

Abstract Purpose: Both ammonia oxidizing archaea (AOA) and bacteria (AOB) perform the ammonia oxidation together. These two kinds of microbes present a convenient model for studying niche specialization. To date, few surveys concentrated on the influence of oxygen concentration on niche specialization of AOA and AOB in intertidal zones. Methods: Here, high-throughput sequencing by Illumina MiSeq and qPCR were applied to detect the change of abundance, diversity as well as community structure of both AOA and AOB with 0-60 cm sediments depth in the intertidal zone in Qingdao.Results and Conclusion: The AOA/AOB amoA gene copy numbers and AOA/AOB OTU numbers were all increased as sediment depth went deeper, which indicated that AOA were more adaptive to oxygen-limited niches compared to AOB and oxygen indeed led to the niche specialization of AOA and AOB in intertidal sediments. The dominant AOA and AOB were the Nitrosopumilus and Nitrosospira clusters, respectively, which indicated an ecological success in intertidal zone. Oxidation-reduction potential (ORP) was significantly positively correlated with AOB abundance and AOB OTU numbers (P < 0.01). In addition, both TN (P < 0.01) and pH (P < 0.05) were significantly and negatively correlated with AOB abundance. TN was also significantly and negatively correlated with AOB OTU numbers (P < 0.05).

Download Full-text

Competition of Ammonia-Oxidizing Archaea and Bacteria from Freshwater Environments

Applied and Environmental Microbiology ◽

10.1128/aem.01038-21 ◽

2021 ◽

Author(s):

Elizabeth French ◽

Jessica A. Kozlowski ◽

Annette Bollmann

Keyword(s):

Ammonia Oxidation ◽

Heterotrophic Bacteria ◽

Ammonia Oxidizer ◽

Ammonium Concentration ◽

Natural Environments ◽

Ammonia Oxidizing Bacteria ◽

Ammonia Oxidizers ◽

Batch Cultures ◽

Freshwater Systems ◽

Ammonia Oxidizing Archaea

In the environment, nutrients are rarely available in constant supply. Therefore, microorganisms require strategies to compete for limiting nutrients. In freshwater systems, ammonia-oxidizing archaea (AOA) and bacteria (AOB) compete with heterotrophic bacteria, photosynthetic microorganisms, and each other for ammonium, which AOA and AOB utilize as their sole source of energy and nitrogen. We investigated the competition between highly enriched cultures of an AOA (AOA-AC1) and an AOB (AOB-G5-7) for ammonium. Based on the amoA gene, the newly enriched archaeal ammonia oxidizer in AOA-AC1 was closely related to Nitrosotenuis spp. and the bacterial ammonia oxidizer in AOB-G5-7, Nitrosomonas sp. Is79, belonged to the Nitrosomonas oligotropha group ( Nitrosomonas cluster 6a). Growth experiments in batch cultures showed that AOB-G5-7 had higher growth rates than AOA-AC1 at higher ammonium concentrations. During chemostat competition experiments under ammonium-limiting conditions, AOA-AC1 dominated the cultures, while AOB-G5-7 decreased in abundance. In batch cultures, the outcome of the competition between AOA and AOB was determined by the initial ammonium concentrations. AOA-AC1 was the dominant ammonia oxidizer at an initial ammonium concentration of 50 μM and AOB-G5-7 at 500 μM. These findings indicate that, during direct competition, AOA-AC1 was able to use ammonium that was unavailable to AOB-G5-7, while AOB-G5-7 dominated at higher ammonium concentrations. The results are in strong accordance with environmental survey data suggesting that AOA are mainly responsible for ammonia oxidation under more oligotrophic conditions, whereas AOB dominate under eutrophic conditions. Importance Nitrification is an important process in the global nitrogen cycle. The first step - ammonia oxidation to nitrite – can be carried out by Ammonia-oxidizing Archaea (AOA) and Ammonia-oxidizing Bacteria (AOB). In many natural environments, these ammonia oxidizers coexist. Therefore, it is important to understand the population dynamics in response to increasing ammonium concentrations. Here, we study the competition between AOA and AOB enriched from freshwater systems. The results demonstrate that AOA are more abundant in systems with low ammonium availabilities and AOB when the ammonium availability increases. These results will help to predict potential shifts in community composition of ammonia oxidizers in the environment due to changes in ammonium availability.

Download Full-text

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

Environmental Microbiology ◽

10.1111/1462-2920.12677 ◽

2015 ◽

Vol 17 (7) ◽

pp. 2261-2274 ◽

Cited By ~ 96

Author(s):

Willm Martens-Habbena ◽

Wei Qin ◽

Rachel E. A. Horak ◽

Hidetoshi Urakawa ◽

Andrew J. Schauer ◽

...

Keyword(s):

Nitric Oxide ◽

Ammonia Oxidation ◽

Ammonia Oxidizing Archaea ◽

Archaeal Ammonia Oxidation

Download Full-text

Effects of Zeolite and Biochar Addition on Ammonia-Oxidizing Bacteria and Ammonia-Oxidizing Archaea Communities during Agricultural Waste Composting

Sustainability ◽

10.3390/su12166336 ◽

2020 ◽

Vol 12 (16) ◽

pp. 6336 ◽

Cited By ~ 1

Author(s):

Xin Wu ◽

Liheng Ren ◽

Jiachao Zhang ◽

Hui Peng

Keyword(s):

Enzyme Activity ◽

Ammonia Oxidation ◽

Agricultural Waste ◽

Amoa Gene ◽

Enzyme Linked Immunosorbent Assay ◽

Ammonia Oxidizing Bacteria ◽

Ammonia Monooxygenase ◽

Gene Abundance ◽

Ammonia Oxidizing Archaea ◽

The Relationship

The effects of zeolite and biochar addition on ammonia-oxidizing bacteria (AOB) and archaea (AOA) communities during agricultural waste composting were determined in this study. Four treatments were conducted as follows: Treatment A as the control with no additive, Treatment B with 5% of zeolite, Treatment C with 5% of biochar, and Treatment D with 5% of zeolite and 5% biochar, respectively. The AOB and AOA amoA gene abundance as well as the ammonia monooxygenase (AMO) activity were estimated by quantitative PCR and enzyme-linked immunosorbent assay, respectively. The relationship between gene abundance and AMO enzyme activity was determined by regression analysis. Results indicated that the AOB was more abundant than that of AOA throughout the composting process. Addition of biochar and its integrated application with zeolite promoted the AOB community abundance and AMO enzyme activity. Significant positive relationships were obtained between AMO enzyme activity and AOB community abundance (r2 = 0.792; P < 0.01) and AOA community abundance (r2 = 0.772; P < 0.01), indicating that both bacteria and archaea played significant roles in microbial ammonia oxidation during composting. Using biochar and zeolite might promote the nitrification activity by altering the sample properties during agricultural waste composting.

Download Full-text