Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium

Nitrous oxide (N<sub>2</sub>O) is a trace gas that contributes to the greenhouse effect and stratospheric ozone depletion. The N<sub>2</sub>O yield from nitrification (moles N<sub>2</sub>O-N produced per mole ammonium-N consumed) has been used to estimate marine N<sub>2</sub>O production rates from measured nitrification rates and global estimates of oceanic export production. However, the N<sub>2</sub>O yield from nitrification is not constant. Previous culture-based measurements indicate that N<sub>2</sub>O yield increases as oxygen (O<sub>2</sub>) concentration decreases and as nitrite (NO<sub>2</sub><sup>−</sup>) concentration increases. Here, we have measured yields of N<sub>2</sub>O from cultures of the marine β-proteobacterium <i>Nitrosomonas marina</i> C-113a as they grew on low-ammonium (50 μM) media. These yields, which were typically between 4 × 10<sup>−4</sup> and 7 × 10<sup>−4</sup> for cultures with cell densities between 2 × 10<sup>2</sup> and 2.1 × 10<sup>4</sup> cells ml<sup>−1</sup>, were lower than previous reports for ammonia-oxidizing bacteria. The observed impact of O<sub>2</sub> concentration on yield was also smaller than previously reported under all conditions except at high starting cell densities (1.5 × 10<sup>6</sup> cells ml<sup>−1</sup>), where 160-fold higher yields were observed at 0.5% O<sub>2</sub> (5.1 μM dissolved O<sub>2</sub>) compared with 20% O<sub>2</sub> (203 μM dissolved O<sub>2</sub>). At lower cell densities (2 × 10<sup>2</sup> and 2.1 × 10<sup>4</sup> cells ml<sup>−1</sup>), cultures grown under 0.5% O<sub>2</sub> had yields that were only 1.25- to 1.73-fold higher than cultures grown under 20% O<sub>2</sub>. Thus, previously reported many-fold increases in N<sub>2</sub>O yield with dropping O<sub>2</sub> could be reproduced only at cell densities that far exceeded those of ammonia oxidizers in the ocean. The presence of excess NO<sub>2</sub><sup>−</sup> (up to 1 mM) in the growth medium also increased N<sub>2</sub>O yields by an average of 70% to 87% depending on O<sub>2</sub> concentration. We made stable isotopic measurements on N<sub>2</sub>O from these cultures to identify the biochemical mechanisms behind variations in N<sub>2</sub>O yield. Based on measurements of δ<sup>15</sup>N<sup>bulk</sup>, site preference (SP = δ<sup>15</sup>N<sup>α</sup>−δ<sup>15</sup>N<sup>β</sup>), and δ<sup>18</sup>O of N<sub>2</sub>O (δ<sup>18</sup>O-N<sub>2</sub>O), we estimate that nitrifier-denitrification produced between 11% and 26% of N<sub>2</sub>O from cultures grown under 20% O<sub>2</sub> and 43% to 87% under 0.5% O<sub>2</sub>. We also demonstrate that a positive correlation between SP and δ<sup>18</sup>O-N<sub>2</sub>O is expected when nitrifying bacteria produce N<sub>2</sub>O. A positive relationship between SP and δ<sup>18</sup>O-N<sub>2</sub>O has been observed in environmental N<sub>2</sub>O datasets, but until now, explanations for the observation invoked only denitrification. Such interpretations may overestimate the role of heterotrophic denitrification and underestimate the role of ammonia oxidation in environmental N<sub>2</sub>O production.

Abstract licence: CC BY

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