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

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 (NH 4 + ) to dinitrogen gas (N 2 ) using intracellular electron acceptors such as nitrite (NO 2 − ) or ni...

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Published inNature communications Vol. 11; no. 1; pp. 2058 - 12
Main Authors Shaw, Dario R., Ali, Muhammad, Katuri, Krishna P., Gralnick, Jeffrey A., Reimann, Joachim, Mesman, Rob, van Niftrik, Laura, Jetten, Mike S. M., Saikaly, Pascal E.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 28.04.2020
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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 (NH 4 + ) to dinitrogen gas (N 2 ) using intracellular electron acceptors such as nitrite (NO 2 − ) 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 NH 4 + with transfer of electrons to insoluble extracellular electron acceptors such as graphene oxide or electrodes in microbial electrolysis cells. 15 N-labeling experiments revealed that NH 4 + was oxidized to N 2 via hydroxylamine (NH 2 OH) as intermediate, and comparative transcriptomics analysis revealed an alternative pathway for NH 4 + oxidation with electrode as electron acceptor. Complete NH 4 + oxidation to N 2 without accumulation of NO 2 − and NO 3 − 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. Bacteria capable of anaerobic ammonium oxidation (anammox) produce half of the nitrogen gas in the atmosphere, but much of their physiology is still unknown. Here the authors show that anammox bacteria are capable of a novel mechanism of ammonium oxidation using extracellular electron transfer.
AbstractList 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 (NH ) to dinitrogen gas (N ) using intracellular electron acceptors such as nitrite (NO ) 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 NH with transfer of electrons to insoluble extracellular electron acceptors such as graphene oxide or electrodes in microbial electrolysis cells. N-labeling experiments revealed that NH was oxidized to N via hydroxylamine (NH OH) as intermediate, and comparative transcriptomics analysis revealed an alternative pathway for NH oxidation with electrode as electron acceptor. Complete NH oxidation to N without accumulation of NO and NO 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.
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 (NH 4 + ) to dinitrogen gas (N 2 ) using intracellular electron acceptors such as nitrite (NO 2 − ) 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 NH 4 + with transfer of electrons to insoluble extracellular electron acceptors such as graphene oxide or electrodes in microbial electrolysis cells. 15 N-labeling experiments revealed that NH 4 + was oxidized to N 2 via hydroxylamine (NH 2 OH) as intermediate, and comparative transcriptomics analysis revealed an alternative pathway for NH 4 + oxidation with electrode as electron acceptor. Complete NH 4 + oxidation to N 2 without accumulation of NO 2 − and NO 3 − 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.
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.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.
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 (NH 4 + ) to dinitrogen gas (N 2 ) using intracellular electron acceptors such as nitrite (NO 2 − ) 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 NH 4 + with transfer of electrons to insoluble extracellular electron acceptors such as graphene oxide or electrodes in microbial electrolysis cells. 15 N-labeling experiments revealed that NH 4 + was oxidized to N 2 via hydroxylamine (NH 2 OH) as intermediate, and comparative transcriptomics analysis revealed an alternative pathway for NH 4 + oxidation with electrode as electron acceptor. Complete NH 4 + oxidation to N 2 without accumulation of NO 2 − and NO 3 − 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. Bacteria capable of anaerobic ammonium oxidation (anammox) produce half of the nitrogen gas in the atmosphere, but much of their physiology is still unknown. Here the authors show that anammox bacteria are capable of a novel mechanism of ammonium oxidation using extracellular electron transfer.
Bacteria capable of anaerobic ammonium oxidation (anammox) produce half of the nitrogen gas in the atmosphere, but much of their physiology is still unknown. Here the authors show that anammox bacteria are capable of a novel mechanism of ammonium oxidation using extracellular electron transfer.
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.Bacteria capable of anaerobic ammonium oxidation (anammox) produce half of the nitrogen gas in the atmosphere, but much of their physiology is still unknown. Here the authors show that anammox bacteria are capable of a novel mechanism of ammonium oxidation using extracellular electron transfer.
ArticleNumber 2058
Author Ali, Muhammad
van Niftrik, Laura
Katuri, Krishna P.
Reimann, Joachim
Jetten, Mike S. M.
Saikaly, Pascal E.
Mesman, Rob
Gralnick, Jeffrey A.
Shaw, Dario R.
Author_xml – sequence: 1
  givenname: Dario R.
  surname: Shaw
  fullname: Shaw, Dario R.
  organization: Water Desalination and Reuse Center (WDRC), Biological and Environmental Science & Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
– sequence: 2
  givenname: Muhammad
  surname: Ali
  fullname: Ali, Muhammad
  organization: Water Desalination and Reuse Center (WDRC), Biological and Environmental Science & Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
– sequence: 3
  givenname: Krishna P.
  surname: Katuri
  fullname: Katuri, Krishna P.
  organization: Water Desalination and Reuse Center (WDRC), Biological and Environmental Science & Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
– sequence: 4
  givenname: Jeffrey A.
  orcidid: 0000-0001-9250-7770
  surname: Gralnick
  fullname: Gralnick, Jeffrey A.
  organization: BioTechnology Institute and Department of Plant and Microbial Biology, University of Minnesota
– sequence: 5
  givenname: Joachim
  surname: Reimann
  fullname: Reimann, Joachim
  organization: Department of Microbiology, Institute for Water and Wetland Research (IWWR), Faculty of Science, Radboud University
– sequence: 6
  givenname: Rob
  orcidid: 0000-0003-0877-3676
  surname: Mesman
  fullname: Mesman, Rob
  organization: Department of Microbiology, Institute for Water and Wetland Research (IWWR), Faculty of Science, Radboud University
– sequence: 7
  givenname: Laura
  orcidid: 0000-0002-7011-7234
  surname: van Niftrik
  fullname: van Niftrik, Laura
  organization: Department of Microbiology, Institute for Water and Wetland Research (IWWR), Faculty of Science, Radboud University
– sequence: 8
  givenname: Mike S. M.
  surname: Jetten
  fullname: Jetten, Mike S. M.
  organization: Department of Microbiology, Institute for Water and Wetland Research (IWWR), Faculty of Science, Radboud University
– sequence: 9
  givenname: Pascal E.
  orcidid: 0000-0001-7678-3986
  surname: Saikaly
  fullname: Saikaly, Pascal E.
  email: pascal.saikaly@kaust.edu.sa
  organization: Water Desalination and Reuse Center (WDRC), Biological and Environmental Science & Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST)
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32345973$$D View this record in MEDLINE/PubMed
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Snippet Anaerobic ammonium oxidation (anammox) bacteria contribute significantly to the global nitrogen cycle and play a major role in sustainable wastewater...
Bacteria capable of anaerobic ammonium oxidation (anammox) produce half of the nitrogen gas in the atmosphere, but much of their physiology is still unknown....
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Ammonia-oxidizing bacteria
Ammonium
Ammonium Compounds - metabolism
Anaerobic processes
Anaerobiosis
Bacteria
Bacteria - metabolism
Electrochemistry
Electrodes
Electrolysis
Electrolytic cells
Electron transfer
Electron Transport
Electrons
Energy efficiency
Extracellular Space - metabolism
Graphene
Humanities and Social Sciences
Hydroxylamine
Microorganisms
multidisciplinary
Nitric oxide
Nitrogen
Nitrogen cycle
Nitrogen dioxide
Oxidation
Oxidation-Reduction
Science
Science (multidisciplinary)
Time Factors
Wastewater treatment
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Title Extracellular electron transfer-dependent anaerobic oxidation of ammonium by anammox bacteria
URI https://link.springer.com/article/10.1038/s41467-020-16016-y
https://www.ncbi.nlm.nih.gov/pubmed/32345973
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https://www.proquest.com/docview/2396308329
https://pubmed.ncbi.nlm.nih.gov/PMC7188810
https://doaj.org/article/5d457f0525ae473ea2f1f2684749ae2f
Volume 11
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