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1. Nitrous oxide reduction by two partial denitrifying bacteria requires denitrification intermediates that cannot be respired

   LaSarre, B; Morlen, R; Neumann, GC; Harwood, CS; McKinlay, JB (September 2023, bioRxiv)

   Denitrification is a form of anaerobic respiration wherein nitrate (NO3-) is sequentially reduced via nitrite (NO2-), nitric oxide, and nitrous oxide (N2O) to dinitrogen gas (N2) by four reductase enzymes. Partial denitrifying bacteria possess only one, or some, of these four reductases and use them as independent respiratory modules. However, it is unclear if partial denitrifiers sense and respond to denitrification intermediates outside of their reductase repertoire. Here we tested the denitrifying capabilities of two purple nonsulfur bacteria, Rhodopseudomonas palustris CGA0092 and Rhodobacter capsulatus SB1003. Each had denitrifying capabilities that matched their genome annotation; CGA0092 reduced NO2- to N2 and SB1003 reduced N2O to N2. For each bacterium, N2O reduction could be used for both electron balance during growth on electron-rich organic compounds in light and for energy transformation via respiration in the dark. However, N2O reduction required supplementation with a denitrification intermediate, including those for which there was no associated denitrification enzyme. For CGA0092, NO3- served as a stable, non-catalyzable molecule that was sufficient to activate N2O reduction. Using a β-galactosidase reporter we found that NO3- acted, at least in part, by stimulating N2O reductase gene expression. In SB1003, NO2-, but not NO3-, activated N2O reduction but NO2- was slowly removed, likely by a promiscuous enzyme activity. Our findings reveal that partial denitrifiers can still be subject to regulation by denitrification intermediates that they cannot use. 

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2. Physicochemical perturbation increases nitrous oxide production from denitrification in soils and sediments

   https://doi.org/10.5194/bg-21-4837-2024  

   Weston, Nathaniel B; Troy, Cynthia; Kearns, Patrick J; Bowen, Jennifer L; Porubsky, William; Hyacinthe, Christelle; Meile, Christof; Van_Cappellen, Philippe; Joye, Samantha B (January 2024, Biogeosciences)

   Abstract. Atmospheric concentrations of nitrous oxide (N2O), a potent greenhouse gas that is also responsible for significant stratospheric ozone depletion, have increased in response to the intensified use of agricultural fertilizers and other human activities that have accelerated nitrogen cycling processes. Microbial denitrification in soils and sediments is a major source of N2O, produced as an intermediate during the reduction of oxidized forms of nitrogen to dinitrogen gas (N2). Substrate availability (nitrate and organic matter) and environmental factors such as oxygen levels, temperature, moisture, and pH influence rates of denitrification and N2O production. Here we describe the role of physicochemical perturbation (defined here as a change from the ambient environmental conditions) in influencing rates of denitrification and N2O production. Changes in salinity, temperature, moisture, pH, and zinc in agricultural soils induced a short-term perturbation response characterized by lower rates of total denitrification and higher rates of net N2O production. The ratio of N2O to total denitrification (N2O : DNF) increased strongly with physicochemical perturbation. A salinity press experiment on tidal freshwater marsh soils revealed that increased N2O production was likely driven by transcriptional inhibition of the nitrous oxide reductase (nos) gene and that the microbial community adapted to altered salinity over a relatively short time frame (within 1 month). Perturbation appeared to confer resilience to subsequent disturbance, and denitrifiers from an environment without salinity fluctuations (tidal freshwater estuarine sediments) demonstrated a stronger N2O perturbation response than denitrifiers from environments with more variable salinity (oligohaline and mesohaline estuarine sediments), suggesting that the denitrifying community from physicochemically stable environments may have a stronger perturbation response. These findings provide a framework for improving our understanding of the dynamic nature of N2O production in soils and sediments, in which changes in physical and/or chemical conditions initiate a short-term perturbation response that promotes N2O production that moderates over time and with subsequent physicochemical perturbation. 

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3. Partitioning of the denitrification pathway and other nitrite metabolisms within global oxygen deficient zones

   https://doi.org/10.1038/s43705-023-00284-y  

   Zhang, Irene H.; Sun, Xin; Jayakumar, Amal; Fortin, Samantha G.; Ward, Bess B.; Babbin, Andrew R. (December 2023, ISME Communications)

   Abstract Oxygen deficient zones (ODZs) account for about 30% of total oceanic fixed nitrogen loss via processes including denitrification, a microbially mediated pathway proceeding stepwise from NO 3 – to N 2 . This process may be performed entirely by complete denitrifiers capable of all four enzymatic steps, but many organisms possess only partial denitrification pathways, either producing or consuming key intermediates such as the greenhouse gas N 2 O. Metagenomics and marker gene surveys have revealed a diversity of denitrification genes within ODZs, but whether these genes co-occur within complete or partial denitrifiers and the identities of denitrifying taxa remain open questions. We assemble genomes from metagenomes spanning the ETNP and Arabian Sea, and map these metagenome-assembled genomes (MAGs) to 56 metagenomes from all three major ODZs to reveal the predominance of partial denitrifiers, particularly single-step denitrifiers. We find niche differentiation among nitrogen-cycling organisms, with communities performing each nitrogen transformation distinct in taxonomic identity and motility traits. Our collection of 962 MAGs presents the largest collection of pelagic ODZ microorganisms and reveals a clearer picture of the nitrogen cycling community within this environment. 

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4. Bacterial denitrification drives elevated N ₂ O emissions in arid southern California drylands

   https://doi.org/10.1126/sciadv.adj1989  

   Krichels, Alexander H; Jenerette, G Darrel; Shulman, Hannah; Piper, Stephanie; Greene, Aral C; Andrews, Holly M; Botthoff, Jon; Sickman, James O; Aronson, Emma L; Homyak, Peter M (December 2023, Science Advances)

   Soils are the largest source of atmospheric nitrous oxide (N₂O), a powerful greenhouse gas. Dry soils rarely harbor anoxic conditions to favor denitrification, the predominant N₂O-producing process, yet, among the largest N₂O emissions have been measured after wetting summer-dry desert soils, raising the question: Can denitrifiers endure extreme drought and produce N₂O immediately after rainfall? Using isotopic and molecular approaches in a California desert, we found that denitrifiers produced N₂O within 15 minutes of wetting dry soils (site preference = 12.8 ± 3.92 per mil, δ¹⁵N^bulk= 18.6 ± 11.1 per mil). Consistent with this finding, we detected nitrate-reducing transcripts in dry soils and found that inhibiting microbial activity decreased N₂O emissions by 59%. Our results suggest that despite extreme environmental conditions—months without precipitation, soil temperatures of ≥40°C, and gravimetric soil water content of <1%—bacterial denitrifiers can account for most of the N₂O emitted when dry soils are wetted. 

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5. Ecological dynamics explain modular denitrification in the ocean

   https://doi.org/10.1073/pnas.2417421121  

   Sun, Xin; Buchanan, Pearse J; Zhang, Irene H; San_Roman, Magdalena; Babbin, Andrew R; Zakem, Emily J (December 2024, Proceedings of the National Academy of Sciences)

   Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO₃^–→NO₂^–→NO→N₂O→N₂), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N₂O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets (“modules”) of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO₂^–and N₂O in a NO₃^–-filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO₃^–→NO₂^–module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO₃^–→NO₂^–module. Results also capture observations that NO₃^–is the dominant source of N₂O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments. 

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