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Extracellular electron transfer-dependent anaerobic oxidation of ammonium by anammox bacteria.

ABSTRACT: Anaerobic ammonium oxidation (anammox) bacteria contribute significantly to the global nitrogen cycle and play a major role in sustainable wastewater treatment. Anammox bacteria convert ammonium (NH₄⁺) to dinitrogen gas (N₂) using intracellular electron acceptors such as nitrite (NO₂^-) or nitric oxide (NO). However, it is still unknown whether anammox bacteria have extracellular electron transfer (EET) capability with transfer of electrons to insoluble extracellular electron acceptors. Here we show that freshwater and marine anammox bacteria couple the oxidation of NH₄⁺ with transfer of electrons to insoluble extracellular electron acceptors such as graphene oxide or electrodes in microbial electrolysis cells. ¹⁵N-labeling experiments revealed that NH₄⁺ was oxidized to N₂ via hydroxylamine (NH₂OH) as intermediate, and comparative transcriptomics analysis revealed an alternative pathway for NH₄⁺ oxidation with electrode as electron acceptor. Complete NH₄⁺ oxidation to N₂ without accumulation of NO₂^- and NO₃^- was achieved in EET-dependent anammox. These findings are promising in the context of implementing EET-dependent anammox process for energy-efficient treatment of nitrogen.

SUBMITTER: Shaw DR

PROVIDER: S-EPMC7188810 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria.

Project description:We examined nitrate-dependent Fe(2+) oxidation mediated by anaerobic ammonium oxidation (anammox) bacteria. Enrichment cultures of "Candidatus Brocadia sinica" anaerobically oxidized Fe(2+) and reduced NO3(-) to nitrogen gas at rates of 3.7 ± 0.2 and 1.3 ± 0.1 (mean ± standard deviation [SD]) nmol mg protein(-1) min(-1), respectively (37°C and pH 7.3). This nitrate reduction rate is an order of magnitude lower than the anammox activity of "Ca. Brocadia sinica" (10 to 75 nmol NH4(+) mg protein(-1) min(-1)). A (15)N tracer experiment demonstrated that coupling of nitrate-dependent Fe(2+) oxidation and the anammox reaction was responsible for producing nitrogen gas from NO3(-) by "Ca. Brocadia sinica." The activities of nitrate-dependent Fe(2+) oxidation were dependent on temperature and pH, and the highest activities were seen at temperatures of 30 to 45°C and pHs ranging from 5.9 to 9.8. The mean half-saturation constant for NO3(-) ± SD of "Ca. Brocadia sinica" was determined to be 51 ± 21 μM. Nitrate-dependent Fe(2+) oxidation was further demonstrated by another anammox bacterium, "Candidatus Scalindua sp.," whose rates of Fe(2+) oxidation and NO3(-) reduction were 4.7 ± 0.59 and 1.45 ± 0.05 nmol mg protein(-1) min(-1), respectively (20°C and pH 7.3). Co-occurrence of nitrate-dependent Fe(2+) oxidation and the anammox reaction decreased the molar ratios of consumed NO2(-) to consumed NH4(+) (ΔNO2(-)/ΔNH4(+)) and produced NO3(-) to consumed NH4(+) (ΔNO3(-)/ΔNH4(+)). These reactions are preferable to the application of anammox processes for wastewater treatment.

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Project description:Enrichment cultures of anaerobic ammonium oxidation (anammox) bacteria as planktonic cell suspensions are essential for studying their ecophysiology and biochemistry, while their cultivation is still laborious. The present study aimed to cultivate two phylogenetically distinct anammox bacteria, "Candidatus Brocadia sinica" and "Ca. Scalindua sp." in the form of planktonic cells using membrane bioreactors (MBRs). The MBRs were continuously operated for more than 250 d with nitrogen loading rates of 0.48-1.02 and 0.004-0.09 kgN m(-3) d(-1) for "Ca. Brocadia sinica" and "Ca. Scalindua sp.", respectively. Planktonic anammox bacterial cells were successfully enriched (>90%) in the MBRs, which was confirmed by fluorescence in-situ hybridization and 16S rRNA gene sequencing analysis. The decay rate and half-saturation constant for NO2(-) of "Ca. Brocadia sinica" were determined to be 0.0029-0.0081 d(-1) and 0.47 mgN L(-1), respectively, using enriched planktonic cells. The present study demonstrated that MBR enables the culture of planktonic anammox bacterial cells, which are suitable for studying their ecophysiology and biochemistry.

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Project description:Anaerobic ammonium oxidation (anammox), the biochemical process oxidizing ammonium into dinitrogen gas using nitrite as an electron acceptor, has only been recognized for its significant role in the global nitrogen cycle not long ago, and its ubiquitous distribution in a wide range of environments has changed our knowledge about the contributors to the global nitrogen cycle. Currently, several groups of methods are used in detection of anammox bacteria based on their physiological and biochemical characteristics, cellular chemical composition, and both 16S rRNA gene and selective functional genes as biomarkers, including hydrazine oxidoreductase and nitrite reductase encoding genes hzo and nirS, respectively. Results from these methods coupling with advances in quantitative PCR, reverse transcription of mRNA genes and stable isotope labeling have improved our understanding on the distribution, diversity, and activity of anammox bacteria in different environments both natural and engineered ones. In this review, we summarize these methods used in detection of anammox bacteria from various environments, highlight the strengths and weakness of these methods, and also discuss the new development potentials on the existing and new techniques in the future.

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Project description:Nitric oxide (NO) has important functions in biology and atmospheric chemistry as a toxin, signaling molecule, ozone depleting agent and the precursor of the greenhouse gas nitrous oxide (N2O). Although NO is a potent oxidant, and was available on Earth earlier than oxygen, it is unclear whether NO can be used by microorganisms for growth. Anaerobic ammonium-oxidizing (anammox) bacteria couple nitrite reduction to ammonium oxidation with NO and hydrazine as intermediates, and produce N2 and nitrate. Here, we show that the anammox bacterium Kuenenia stuttgartiensis is able to grow in the absence of nitrite by coupling ammonium oxidation to NO reduction, and produce only N2. Under these growth conditions, the transcription of proteins necessary for NO generation is downregulated. Our work has potential implications in the control of N2O and NO emissions from natural and manmade ecosystems, where anammox bacteria contribute significantly to N2 release to the atmosphere. We hypothesize that microbial NO-dependent ammonium oxidation may have existed on early Earth.

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Anammox Bacteria Are Potentially Involved in Anaerobic Ammonium Oxidation Coupled to Iron(III) Reduction in the Wastewater Treatment System.

Project description:Anaerobic ammonium oxidation coupled to nitrite reduction (termed as Anammox) was demonstrated as an efficient pathway to remove nitrogen from a wastewater treatment system. Recently, anaerobic ammonium oxidation was also identified to be linked to iron(III) reduction (termed Feammox) with dinitrogen, nitrite, or nitrate as end-product, reporting to enhance nitrogen removal from the wastewater treatment system. However, little is known about the role of Anammox bacteria in the Feammox process. Here, slurry from wastewater reactor amended with ferrihydrite was employed to investigate activity of Anammox bacteria in the Feammox process using the 15N isotopic tracing technique combined with 16S rRNA gene amplicon sequencing. A significantly positive relationship between rates of 15N2 production and iron(III) reduction indicated the occurrence of Feammox during incubation. Relative abundances of Anammox bacteria including Brocadia, Kuenenia, Jettenia, and unclassified Brocadiaceae were detected with low relative abundances, whereas Geobacteraceae dominated in the treatment throughout the incubation. 15N2 production rates significantly positively correlated with relative abundances of Geobacter, unclassified Geobacteraceae, and Anammox bacteria, revealing their contribution to nitrogen generation via Feammox. Overall, these findings suggested Anammox bacteria or cooperation between Anammox bacteria and iron(III) reducers serves a potential role in Feammox process.

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