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Dual nitrogen and oxygen isotope fractionation during anaerobic ammonium oxidation by anammox bacteria.

ABSTRACT: Natural abundance of stable nitrogen (N) and oxygen (O) isotopes are invaluable biogeochemical tracers for assessing the N transformations in the environment. To fully exploit these tracers, the N and O isotope effects (¹⁵? and ¹⁸?) associated with the respective nitrogen transformation processes must be known. However, the N and O isotope effects of anaerobic ammonium oxidation (anammox), one of the major fixed N sinks and NO₃^- producers, are not well known. Here, we report the dual N and O isotope effects associated with anammox by three different anammox bacteria including "Ca. Scalindua japonica", a putative marine species, which were measured in continuous enrichment culture experiments. All three anammox species yielded similar N isotope effects of NH₄⁺ oxidation to N₂ (¹⁵?_NH4?N2) ranging from 30.9‰ to 32.7‰ and inverse kinetic isotope effects of NO₂^- oxidation to NO₃^- (¹⁵?_NO2?NO3?=?-45.3‰ to -30.1‰). In contrast, ¹⁵?_NO2?N2 (NO₂^- reduction to N₂) were significantly different among three species, which is probably because individual anammox bacteria species might possess different types of nitrite reductase. We also report the combined O isotope effects for NO₂^- oxidation (¹⁸E_NO2?NO3) by anammox bacteria. These obtained dual N and O isotopic effects could provide significant insights into the contribution of anammox bacteria to the fixed N loss and NO₂^- reoxidation (N recycling) in various natural environments.

SUBMITTER: Kobayashi K

PROVIDER: S-EPMC6775995 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Dual nitrogen and oxygen isotope fractionation during anaerobic ammonium oxidation by anammox bacteria.

Kobayashi Kanae K Makabe Akiko A Yano Midori M Oshiki Mamoru M Kindaichi Tomonori T Casciotti Karen L KL Okabe Satoshi S

The ISME journal 20190528 10

Natural abundance of stable nitrogen (N) and oxygen (O) isotopes are invaluable biogeochemical tracers for assessing the N transformations in the environment. To fully exploit these tracers, the N and O isotope effects (15ε and 18ε) associated with the respective nitrogen transformation processes must be known. However, the N and O isotope effects of anaerobic ammonium oxidation (anammox), one of the major fixed N sinks and NO3- producers, are not well ...[more]

PMID: 31138875

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Project description:The naturally occurring nitrogen (N) isotopes, 15N and 14N, exhibit different reaction rates during many microbial N transformation processes, which results in N isotope fractionation. Such isotope effects are critical parameters for interpreting natural stable isotope abundances as proxies for biological process rates in the environment across scales. The kinetic isotope effect of ammonia oxidation (AO) to nitrite (NO2 -), performed by ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB), is generally ascribed to the enzyme ammonia monooxygenase (AMO), which catalyzes the first step in this process. However, the kinetic isotope effect of AMO, or ε A M O , has been typically determined based on isotope kinetics during product formation (cumulative product, NO2 -) alone, which may have overestimated ε A M O due to possible accumulation of chemical intermediates and alternative sinks of ammonia/ammonium (NH3/NH4 +). Here, we analyzed 15N isotope fractionation during archaeal ammonia oxidation based on both isotopic changes in residual substrate (RS, NH4 +) and cumulative product (CP, NO2 -) pools in pure cultures of the soil strain Nitrososphaera viennensis EN76 and in highly enriched cultures of the marine strain Nitrosopumilus adriaticus NF5, under non-limiting substrate conditions. We obtained ε A M O values of 31.9-33.1‰ for both strains based on RS (δ15NH4 +) and showed that estimates based on CP (δ15NO2 -) give larger isotope fractionation factors by 6-8‰. Complementary analyses showed that, at the end of the growth period, microbial biomass was 15N-enriched (10.1‰), whereas nitrous oxide (N2O) was highly 15N depleted (-38.1‰) relative to the initial substrate. Although we did not determine the isotope effect of NH4 + assimilation (biomass formation) and N2O production by AOA, our results nevertheless show that the discrepancy between ε A M O estimates based on RS and CP might have derived from the incorporation of 15N-enriched residual NH4 + after AMO reaction into microbial biomass and that N2O production did not affect isotope fractionation estimates significantly.

Dataset Information

Dual nitrogen and oxygen isotope fractionation during anaerobic ammonium oxidation by anammox bacteria.

Publications

Dual nitrogen and oxygen isotope fractionation during anaerobic ammonium oxidation by anammox bacteria.

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