Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils

Sanford, Robert A.; Wagner, Darlene; Wu, Qingzhong; Chee‐Sanford, Joanne C.; Thomas, Sara H.; Cruz-García, Claribel; Rodríguez, Gina; Massol-Deyá, Arturo; Krishnani, Kishore Kumar; Ritalahti, Kirsti M.; Nissen, Silke; Konstantinidis, Konstantinos T.; Löffler, Frank E.

doi:10.1073/pnas.1211238109

Cited by 543 publications

(574 citation statements)

References 58 publications

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“…Our data suggest that N 2 O accumulation is toxic to cellular metabolism at extracellular concentrations as low as ∼0.1 mmol/L. Thus, NosZ may play a previously unrecognized role in N 2 O resistance in microbial communities and this provides an insight into the function of NosZ in nondenitrifier bacterial genomes (35). The implications are that organisms that live in microbial communities and do not have B 12 -independent mechanisms, or NosZ, could be compromised by the release of N 2 O following incomplete denitrification by partial denitrifiers or during Cu-limitation.…”

Section: Discussionmentioning

confidence: 97%

Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism

Sullivan

Gates

Appia-Ayme

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

125

116

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Global agricultural emissions of the greenhouse gas nitrous oxide (N 2 O) have increased by around 20% over the last 100 y, but regulation of these emissions and their impact on bacterial cellular metabolism are poorly understood. Denitrifying bacteria convert nitrate in soils to inert di-nitrogen gas (N 2 ) via N 2 O and the biochemistry of this process has been studied extensively in Paracoccus denitrificans. Here we demonstrate that expression of the gene encoding the nitrous oxide reductase (NosZ), which converts N 2 O to N 2 , is regulated in response to the extracellular copper concentration. We show that elevated levels of N 2 O released as a consequence of decreased cellular NosZ activity lead to the bacterium switching from vitamin B 12 -dependent to vitamin B 12 -independent biosynthetic pathways, through the transcriptional modulation of genes controlled by vitamin B 12 riboswitches. This inhibitory effect of N 2 O can be rescued by addition of exogenous vitamin B 12 .denitrification | transcription | NosR | NosC G lobal atmospheric loading of the ozone-depleting greenhouse gas, nitrous oxide (N 2 O), is on the increase (1). Molecule for molecule, its radiative potential is ∼300-fold higher than carbon dioxide (2, 3), comprising ∼9% of global radiative forcing by greenhouse gases (4). In addition, atmospheric N 2 O is stable for ∼120 y. Approximately 70% of anthropogenic N 2 O loading arises from agriculture, mainly from the use of nitrogencontaining fertilizers by soil microbes for dissimilatory purposes. Taken together, these features make N 2 O an important target for mitigation strategies (5).N 2 O is an intermediate in the sequential reduction of nitrate (NO 3 − ) to di-nitrogen (N 2 ), via nitrite (NO 2 − ), nitric oxide (NO), and N 2 O, a process known as denitrification (6). Under certain conditions, the final step in denitrification is dispensed with and N 2 O is released into the atmosphere. One limiting factor in this process is copper (Cu) availability, the metal cofactor required by the N 2 O reductase (NosZ) that destroys N 2 O (5, 7, 8). During Cu-limitation the catalytic capacity of the Nos system may be exceeded by the rate of the preceding reactions that generate N 2 O (i.e., NO 3 − , NO 2 − , and NO reduction) and thus, N 2 O is emitted by denitrifying bacteria (7, 9, 10).Much attention has been given to the cytotoxic properties of NO as a free-radical and oxidant, but N 2 O is often described as a relatively inert intermediate of the nitrogen cycle. However, N 2 O exhibits cytotoxicity, as it is known to bind to and inactivate vitamin B 12 (B 12 ), an essential cellular cofactor in B 12 -dependent enzymes involved in methionine and DNA synthesis (11,12). B 12 also acts as a ligand for B 12 riboswitches that modulate gene expression in the absence of this cofactor (13,14). The possible impact of environmental N 2 O emissions on B 12 metabolism in microbiological communities has largely been ignored. As levels of N 2 O increase in the environment, there is a compelling argument for ...

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Section: Discussionmentioning

confidence: 97%

Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism

Sullivan

Gates

Appia-Ayme

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

125

116

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“…Verrucomicrobia are known to be abundant in soils, but their ecological role remains unclear (37,38). The pathway's most abundant genus, Anaeromyxobacter (phylum Deltaproteobacteria), is common in agricultural soil and has recently been shown to carry out a previously unrecognized process of nondenitrifying N 2 O reduction to N 2 (39). The relative abundances of genera encoding the other six N pathways in the soil samples are reported in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Second, assigning function and taxonomy from short-read sequences is limited by genomic databases where annotations in some cases may be sparse and/or erroneous (56,57). The N cycle is an archetype of this problem, because new N processes and lineages continue to be identified (39,(58)(59)(60)(61). Despite these challenges, the application of metagenomic data to a trait-based framework offers a powerful avenue for elucidating the role that microbial communities play in regulating biogeochemical processes (24,62).…”

Section: Discussionmentioning

confidence: 99%

Global biogeography of microbial nitrogen-cycling traits in soil

Nelson

Martiny

2016

Proc. Natl. Acad. Sci. U.S.A.

415

232

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Microorganisms drive much of the Earth’s nitrogen (N) cycle, but we still lack a global overview of the abundance and composition of the microorganisms carrying out soil N processes. To address this gap, we characterized the biogeography of microbial N traits, defined as eight N-cycling pathways, using publically available soil metagenomes. The relative frequency of N pathways varied consistently across soils, such that the frequencies of the individual N pathways were positively correlated across the soil samples. Habitat type, soil carbon, and soil N largely explained the total N pathway frequency in a sample. In contrast, we could not identify major drivers of the taxonomic composition of the N functional groups. Further, the dominant genera encoding a pathway were generally similar among habitat types. The soil samples also revealed an unexpectedly high frequency of bacteria carrying the pathways required for dissimilatory nitrate reduction to ammonium, a little-studied N process in soil. Finally, phylogenetic analysis showed that some microbial groups seem to be N-cycling specialists or generalists. For instance, taxa within the Deltaproteobacteria encoded all eight N pathways, whereas those within the Cyanobacteria primarily encoded three pathways. Overall, this trait-based approach provides a baseline for investigating the relationship between microbial diversity and N cycling across global soils.

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“…Furthermore, two recent studies revealed a physiological dichotomy in the diversity of N 2 O-reducing microorganisms (Sanford et al, 2012;Jones et al, 2013). These recent findings might also be of importance for understanding the relationship between N 2 O reduction and the activity and diversity of N 2 O-reducing microorganisms in biochar-amended soils and should be taken into account in future studies.…”

Section: Discussionmentioning

confidence: 99%

Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community

Harter¹,

Krause²,

Schuettler³

et al. 2013

The ISME Journal

533

258

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Nitrous oxide (N 2 O) contributes 8% to global greenhouse gas emissions. Agricultural sources represent about 60% of anthropogenic N 2 O emissions. Most agricultural N 2 O emissions are due to increased fertilizer application. A considerable fraction of nitrogen fertilizers are converted to N 2 O by microbiological processes (that is, nitrification and denitrification). Soil amended with biochar (charcoal created by pyrolysis of biomass) has been demonstrated to increase crop yield, improve soil quality and affect greenhouse gas emissions, for example, reduce N 2 O emissions. Despite several studies on variations in the general microbial community structure due to soil biochar amendment, hitherto the specific role of the nitrogen cycling microbial community in mitigating soil N 2 O emissions has not been subject of systematic investigation. We performed a microcosm study with a water-saturated soil amended with different amounts (0%, 2% and 10% (w/w)) of high-temperature biochar. By quantifying the abundance and activity of functional marker genes of microbial nitrogen fixation (nifH), nitrification (amoA) and denitrification (nirK, nirS and nosZ) using quantitative PCR we found that biochar addition enhanced microbial nitrous oxide reduction and increased the abundance of microorganisms capable of N 2 -fixation. Soil biochar amendment increased the relative gene and transcript copy numbers of the nosZ-encoded bacterial N 2 O reductase, suggesting a mechanistic link to the observed reduction in N 2 O emissions. Our findings contribute to a better understanding of the impact of biochar on the nitrogen cycling microbial community and the consequences of soil biochar amendment for microbial nitrogen transformation processes and N 2 O emissions from soil.

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Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils

Cited by 543 publications

References 58 publications

Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism

Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism

Global biogeography of microbial nitrogen-cycling traits in soil

Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community

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Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils

Cited by 543 publications

References 58 publications

Copper control of bacterial nitrous oxide emission and its impact on vitamin B 12 -dependent metabolism

Copper control of bacterial nitrous oxide emission and its impact on vitamin B 12 -dependent metabolism

Global biogeography of microbial nitrogen-cycling traits in soil

Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community

Contact Info

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Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism

Copper control of bacterial nitrous oxide emission and its impact on vitamin B ₁₂ -dependent metabolism