Detecting Nitrous Oxide Reductase (
            <i>nosZ</i>
            ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle

Orellana, Luis H.; Rodriguez-R, Luis M.; Higgins, Steven A.; Chee‐Sanford, Joanne C.; Sanford, Robert A.; Ritalahti, Kirsti M.; Löffler, Frank E.; Konstantinidis, Konstantinos T.

doi:10.1128/mbio.01193-14

Cited by 164 publications

(131 citation statements)

References 39 publications

(62 reference statements)

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“…Quantitative PCR data and metagenomic analyses revealed that nosZ genes affiliated with the Anaeromyxobacter genus are abundant in agricultural soils of the U.S. Midwest corn belt (15,19). The results of Anaeromyxobacter genome analyses suggest that members of this genus do not possess NO-forming nitrite reductase genes (nirK or nirS) but share a clade II nosZ gene (15).…”

Section: Discussionmentioning

confidence: 77%

“…Indeed, P. stutzeri had a growth yield 1.8-fold lower than the value measured for Anaeromyxobacter dehalogenans strain 2CP-C. Fast-growing r-strategists are rarely abundant in nutrient-limited soil environments, and the slow-growing K strategists (e.g., Anaeromyxobacter, Opitutus, and Gemmatimonas populations) are generally more robust under such conditions (19,46,47). Competition experiments performed under controlled N 2 O flux conditions will provide further insights and directly reveal the relevance of clade I versus clade II organisms for modulating soil N 2 O emissions.…”

Section: Discussionmentioning

confidence: 98%

“…The genome sequencing efforts indicated that D. denitrificans strain ED-1 does not harbor a clade I nosZ gene but instead possesses a clade II nosZ gene. (19,37). In a fertilized agricultural soil ecosystem, N 2 O concentrations reaching 1,200 ppmv were observed following the application of cattle urine, and elevated N 2 O concentrations exceeding 100 ppmv were sustained for at least 10 days (38).…”

Section: Growthmentioning

confidence: 99%

“…Growth experiments with Anaeromyxobacter dehalogenans, an organism carrying the clade II nosZ, demonstrated that clade II NosZ functions as a respiratory oxidoreductase (15). PCR and metagenome analyses demonstrated the clade II nosZ gene abundance in different soils and suggested a correlation between the abundance and diversity of microorganisms carrying the clade II nosZ and a soil's N 2 O sink capacity (16,18,19).…”

mentioning

confidence: 99%

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Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ

Yoon

Nissen

Park

et al. 2016

Appl Environ Microbiol

169

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Nitrous oxide (N 2 O) is a potent greenhouse gas with a strong potential to drive climate change (1, 2) and will continue to be the largest contributor to ozone depletion in the stratosphere (2, 3). Anthropogenic activities, predominantly, fertilizer application in agricultural production, have contributed to a steady increase in atmospheric N 2 O concentrations, and a continued upward trend is expected (4-6). Particularly troublesome are the findings of a recent study that concluded that without solutions for the N 2 O problem, carbon dioxide (CO 2 ) emission reductions even greater than those already proposed will be required to avoid climate change (7). Due to its environmental impact, the pathways leading to the generation and consumption of N 2 O have received heightened interest.In the environment, N 2 O is predominantly formed as an intermediate of denitrification and a nitrification by-product (8). Denitrification is the stepwise reduction of NO 3 Ϫ /NO 2 Ϫ to gaseous products (i.e., N 2 O, N 2 ), with each step being mediated by distinct enzyme systems (9). A kinetic imbalance in the rates of reactions producing and consuming N 2 O during denitrification leads to the release of N 2 O to the atmosphere (8, 10). In nitrification, N 2 O is generated by nitrifier denitrification and as a byproduct of ammonia oxidation (8,11,12). A recent report indicated that nitrifiers, rather than denitrifiers, may be the primary source of N 2 O in agricultural soils (12). Other processes contributing to N 2 O formation include respiratory ammonification (also known as dissimilatory nitrate/nitrite reduction to ammonium [DNRA]) and chemodenitrification (i.e., the abiotic reaction of NO 2 Ϫ with ferrous iron) (13,14). In contrast to the diverse pathways of N 2 O generation, the only known major biological pathway for the removal of N 2 O is by reduction to N 2 , catalyzed by the enzyme nitrous oxide reductase (NosZ) (8,(15)(16)(17)

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Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 98%

Section: Growthmentioning

confidence: 99%

mentioning

confidence: 99%

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Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ

Yoon

Nissen

Park

et al. 2016

Appl Environ Microbiol

169

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“…Metagenomic analyses of environmental DNA have revealed that clade II nosZ genes are, in fact, abundant in diverse environments, ranging from tropical forest and hot desert to Arctic tundra and polar desert (18,22). Among the most abundant phylogenetic groups of nosZ in the environment are clade II nosZ genes affiliated with the Gemmatimonadetes phylum (16,18).…”

mentioning

confidence: 99%

Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

Park

Kim

Yoon

2017

Appl Environ Microbiol

128

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N 2 O-reducing organisms with nitrous oxide reductases (NosZ) are known as the only biological sink of N 2 O in the environment. Among the most abundant nosZ genes found in the environment are nosZ genes affiliated with the understudied Gemmatimonadetes phylum. In this study, a unique regulatory mechanism of N 2 O reduction in Gemmatimonas aurantiaca strain T-27, an isolate affiliated with the Gemmatimonadetes phylum, was examined. Strain T-27 was incubated with N 2 O and/or O 2 as the electron acceptor. Significant N 2 O reduction was observed only when O 2 was initially present. When batch cultures of strain T-27 were amended with O 2 and N 2 O, N 2 O reduction commenced after O 2 was depleted. In a long-term incubation with the addition of N 2 O upon depletion, the N 2 O reduction rate decreased over time and came to an eventual stop. Spiking of the culture with O 2 resulted in the resuscitation of N 2 O reduction activity, supporting the hypothesis that N 2 O reduction by strain T-27 required the transient presence of O 2 . The highest level of nosZ transcription (8.97 nosZ transcripts/recA transcript) was observed immediately after O 2 depletion, and transcription decreased ϳ25-fold within 85 h, supporting the observed phenotype. The observed difference between responses of strain T-27 cultures amended with and without N 2 O to O 2 starvation suggested that N 2 O helped sustain the viability of strain T-27 during temporary anoxia, although N 2 O reduction was not coupled to growth. The findings in this study suggest that obligate aerobic microorganisms with nosZ genes may utilize N 2 O as a temporary surrogate for O 2 to survive periodic anoxia.IMPORTANCE Emission of N 2 O, a potent greenhouse gas and ozone depletion agent, from the soil environment is largely determined by microbial sources and sinks. N 2 O reduction by organisms with N 2 O reductases (NosZ) is the only known biological sink of N 2 O at environmentally relevant concentrations (up to ϳ1,000 parts per million by volume [ppmv]). Although a large fraction of nosZ genes recovered from soil is affiliated with nosZ found in the genomes of the obligate aerobic phylum Gemmatimonadetes, N 2 O reduction has not yet been confirmed in any of these organisms. This study demonstrates that N 2 O is reduced by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27, and suggests a novel regulation mechanism for N 2 O reduction in this organism, which may also be applicable to other obligate aerobic organisms possessing nosZ genes. We expect that these findings will significantly advance the understanding of N 2 O dynamics in environments with frequent transitions between oxic and anoxic conditions.

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Assembly ofCuZandCuAin Nitrous Oxide Reductase

Pauleta

Moura

2017

Encyclopedia of Inorganic and Bioinorganic Chemistry

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Nitrous oxide (N 2 O) reductase is a copper enzyme that catalyzes the reduction of N 2 O to dinitrogen, the last step of the denitrification pathway. This enzyme has two copper centers: a CuA center that is the electron transfer center and the “CuZ center” where the catalysis occurs. This enzyme has been the center of several studies over the last 20 years, and many of its spectroscopic and catalytic properties have been determined, as well as its structure in different oxidation states. These studies have also revealed that the CuA center is similar to the one present in cytochrome c oxidase, being a binuclear copper center, while the CuZ center is unique in biology, being a tetranuclear copper center bridged by a sulfur atom. Moreover, these studies have also identified that the CuZ center can exist in two forms, CuZ*(4Cu1S) and CuZ(4Cu2S). The first has a high turnover number in the fully reduced state, while the CuZ(4Cu2S) form of CuZ center has a very small turnover number and cannot explain the high capacity of the whole cells in reducing N 2 O, from which the enzyme is isolated with CuZ center mainly in that form. This fact envisages an activation mechanism still to be unraveled that might involve one or more enzymes/proteins encoded by the nos genes and a putative sulfur‐displacement mechanism. The biogenesis of these two centers has not been extensively studied, and at least with respect to the copper insertion, it has been postulated that there are alternative routes. The apo‐N 2 OR is synthesized in the cytoplasm in the apo form and is transported to the periplasmic space by either the Sec (unfolded state) or Tat system (dimer folded state), where the centers are assembled. Thus, CuA assembly has been proposed to be dependent on a copper chaperone, pCu A C, and Sco, a thiol‐disulfide reductase that reduces the disulfide bridge between the two cysteines in the apo‐CuA center. Relative to the CuZ center, the delivery of copper atoms is by NosL, an outer‐membrane protein, while the sulfur atoms are transported by the ABC transporter encoded by nosDFY genes. The other accessory proteins NosR and NosX have been assigned broader functions. NosR has been implicated in nosZ expression, as well as in maintaining the activity of N 2 OR, a function that has been shared by NosX. In this chapter the main biochemical properties of N 2 OR, as well as the biogenesis of its two copper centers, will be reviewed.

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Detecting Nitrous Oxide Reductase ( nosZ ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle

Cited by 164 publications

References 39 publications

Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ

Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ

Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

Assembly ofCuZandCuAin Nitrous Oxide Reductase

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