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Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea Public Deposited

https://ir.library.oregonstate.edu/concern/articles/mg74qn81m

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  • Nitrosomonas europaea is a chemolithoautotrophic bacterium that oxidizes ammonia (NH₃) to obtain energy for growth on carbon dioxide (CO₂) and can also produce nitrous oxide (N₂O), a greenhouse gas. We interrogated the growth, physiological, and transcriptome responses of N. europaea to conditions of replete (>5.2 mM) and limited inorganic carbon (IC) provided by either 1.0 mM or 0.2 mM sodium carbonate (Na₂CO₃) supplemented with atmospheric CO₂. IC-limited cultures oxidized 25 to 58% of available NH₃ to nitrite, depending on the dilution rate and Na₂CO₃ concentration. IC limitation resulted in a 2.3-fold increase in cellular maintenance energy requirements compared to those for NH₃-limited cultures. Rates of N₂O production increased 2.5- and 6.3-fold under the two IC-limited conditions, increasing the percentage of oxidized NH₃-N that was transformed to N₂O-N from 0.5% (replete) up to 4.4% (0.2 mM Na₂CO₃). Transcriptome analysis showed differential expression (P ≤ 0.05) of 488 genes (20% of inventory) between replete and IC-limited conditions, but few differences were detected between the two IC-limiting treatments. IC-limited conditions resulted in a decreased expression of ammonium/ammonia transporter and ammonia monooxygenase subunits and increased the expression of genes involved in C₁ metabolism, including the genes for RuBisCO (cbb gene cluster), carbonic anhydrase, folate-linked metabolism of C₁ moieties, and putative C salvage due to oxygenase activity of RuBisCO. Increased expression of nitrite reductase (gene cluster NE0924 to NE0927) correlated with increased production of N₂O. Together, these data suggest that N. europaea adapts physiologically during IC-limited steady-state growth, which leads to the uncoupling of NH₃ oxidation from growth and increased N₂O production. IMPORTANCE: Nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, is an important process in the global nitrogen cycle. This process is generally dependent on ammonia-oxidizing microorganisms and nitrite-oxidizing bacteria. Most nitrifiers are chemolithoautotrophs that fix inorganic carbon (CO₂) for growth. Here, we investigate how inorganic carbon limitation modifies the physiology and transcriptome of Nitrosomonas europaea, a model ammonia-oxidizing bacterium, and report on increased production of N₂O, a potent greenhouse gas. This study, along with previous work, suggests that inorganic carbon limitation may be an important factor in controlling N₂O emissions from nitrification in soils and wastewater treatment.
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  • Mellbye, B. L., Giguere, A., Chaplen, F., Bottomley, P. J., & Sayavedra-Soto, L. A. (2016). Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea. Applied and environmental microbiology, 82(11), 3310-3318. doi:10.1128/AEM.00294-16
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  • The DOE provided funding to the co-principal investigators L.A.S.-S. and P.J.B. under award ER65192, the USDA provided funding to P.J.B. under USDA-NIFA award 2012-67019-3028, and the NSF provided funding to principal investigator F.C. and co-principal investigator L.A.S.-S. under EAGER award CBET 1239870. During the duration of this project, B.L.M. was partially supported by a USDA-NIFA postdoctoral fellowship, award 2016-67012-24691.
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