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

Dario R. Shaw, Muhammad Ali, Krishna P. Katuri, Jeffrey A. Gralnick, Joachim Reimann, Rob Mesman, Laura van Niftrik, Mike S. M. Jetten, Pascal E. Saikaly

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Dec 19, 2019
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Received Date: 11th December 19

Anaerobic ammonium oxidation (anammox) by anammox bacteria contributes significantly to the global nitrogen cycle, and plays a major role in sustainable wastewater treatment. Anammox bacteria convert ammonium (NH4+) to dinitrogen gas (N2) using nitrite (NO2) or nitric oxide (NO) as the electron acceptor. In the absence of NO2– or NO, anammox bacteria can couple formate oxidation to the reduction of metal oxides such as Fe(III) or Mn(IV). Their genomes contain homologs of Geobacter and Shewanella cytochromes involved in extracellular electron transfer (EET). However, it is still unknown whether anammox bacteria have EET capability and can couple the oxidation of NH4with transfer of electrons to carbon-based insoluble extracellular electron acceptors. Here we show using complementary approaches that in the absence of NO2, freshwater and marine anammox bacteria couple the oxidation of NH4with transfer of electrons to carbon-based insoluble extracellular electron acceptorssuch as graphene oxide (GO) or electrodes poised at a certain potential in microbial electrolysis cells (MECs). Metagenomics, fluorescence in-situ hybridization and electrochemical analyses coupled with MEC performance confirmed that anammox electrode biofilms were responsible for current generation through EET-dependent oxidation of NH4+15N-labelling experiments revealed the molecular mechanism of the EET-dependent anammox process. NH4was oxidized to Nvia hydroxylamine (NH2OH) as intermediate when electrode was the terminal electron acceptor. Comparative transcriptomics analysis supported isotope labelling experiments and revealed an alternative pathway for NH4oxidation coupled to EET when electrode is used as electron acceptor compared to NO2– as electron acceptor. To our knowledge, our results provide the first experimental evidence that marine and freshwater anammox bacteria can couple NH4oxidation with EET, which is a significant finding, and challenges our perception of a key player of anaerobic oxidation of NH4in natural environments and engineered systems.

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This is an abstract of a preprint hosted on an independent third party site. It has not been peer reviewed but is currently under consideration at Nature Communications.

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