Iron assimilation and utilization in anaerobic ammonium oxidizing bacteria

Ferousi, Christina; Lindhoud, Simon; Baymann, Frauke; Kartal, Boran; Jetten, Mike S. M.; Reimann, Joachim

doi:10.1016/j.cbpa.2017.03.009

Cited by 125 publications

(48 citation statements)

References 61 publications

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“…Iron is the fourth most abundant element in Earth’s crust ( 93 ) and plays an essential role in anammox metabolism. Energy conservation in anammox bacteria depends on iron-containing proteins (i.e., cytochromes and iron-sulfur proteins) ( 14 ). Surprisingly the proteins involved in iron transport and assimilation are still unknown.…”

Section: Supplementary Materialsmentioning

confidence: 99%

“…S10, Table S3 and 13). The expressed siderophore-mediated transport system, which was previously believed to be absent in anammox bacteria ( 14 ), is homolog to the well-studied TonB-dependent Fe(III) uptake complex present in Gram-negative bacteria ( 94 ). Fe(III) uptake relies on beta-barrel TonB-dependent receptors in the outer membrane ( 95 ) and an energy-transducing protein complex TonB-ExbB-ExbD that links the outer with the inner membrane and generate a proton motive force ( 94 ).…”

Section: Supplementary Materialsmentioning

confidence: 99%

“…S10, Table S3). After being reduced, the iron can be assimilated into the metalloprosthetic groups of protein complexes ( 14 ). Even though Fe(III) was not added in the experimental setup, Ca .…”

Section: Supplementary Materialsmentioning

confidence: 99%

“…This resonates with a recent finding where Listeria monocytogenes , a host-associated pathogen and fermentative Gram-positive bacterium, was able to respire through a flavin-based EET process and behaved as an electrochemically active microorganism (i.e., able to transfer electrons from oxidized fuel (substrate) to a working electrode via EET process) ( 13 ). Further it was reported that anammox bacteria seem to have homologs of Geobacter and Shewanella multi-heme cytochromes that are responsible for EET ( 14 ). These observations stimulated us to investigate whether anammox bacteria can couple NH 4 + oxidation with EET to carbon-based insoluble extracellular electron acceptor and can behave as electrochemically active bacteria.…”

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confidence: 99%

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

Shaw

Ali

Katuri

et al. 2019

Preprint

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AbstractAnaerobic 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 NH4+ with 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 NH4+ with transfer of electrons to carbon-based insoluble extracellular electron acceptors such 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. NH4+ was oxidized to N2 via hydroxylamine (NH2OH) as intermediate when electrode was the terminal electron acceptor. Comparative transcriptomics analysis supported isotope labelling experiments and revealed an alternative pathway for NH4+ oxidation 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 NH4+ oxidation with EET, which is a significant finding, and challenges our perception of a key player of anaerobic oxidation of NH4+ in natural environments and engineered systems.

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Section: Supplementary Materialsmentioning

confidence: 99%

Section: Supplementary Materialsmentioning

confidence: 99%

Section: Supplementary Materialsmentioning

confidence: 99%

mentioning

confidence: 99%

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

Shaw

Ali

Katuri

et al. 2019

Preprint

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“…J. caeni’ (Ali et al., ), indicating high assimilatory requirements for iron in anammox bacteria cells. Indeed, iron‐containing proteins, especially haem proteins, in anammoxosome play a key role in the energy conservation of anammox bacteria (Ferousi et al ., ; Giessen and Silver ). All the known anammox bacteria genomes carry feo B encoding a membrane‐bound ferrous iron transporter (Fig.…”

Section: Resultsmentioning

confidence: 97%

Genetic diversity of marine anaerobic ammonium‐oxidizing bacteria as revealed by genomic and proteomic analyses of ‘Candidatus Scalindua japonica’

Oshiki

Mizuto

Kimura

et al. 2017

Environ Microbiol Rep

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Anaerobic ammonium-oxidizing (anammox) bacteria affiliated with the genus 'Candidatus Scalindua' are responsible for significant nitrogen loss in oceans, and thus their ecophysiology is of great interest. Here, we enriched a marine anammox bacterium, 'Ca. S. japonica' from a Hiroshima bay sediment in Japan, and comparative genomic and proteomic analyses of 'Ca. S. japonica' were conducted. Sequence of the 4.81-Mb genome containing 4019 coding regions of genes (CDSs) composed of 47 contigs was determined. In the proteome, 1762 out of 4019 CDSs in the 'Ca. S. japonica' genome were detected. Based on the genomic and proteomic data, the core anammox process and carbon fixation of 'Ca. S. japonica' were further investigated. Additionally, the present study provides the first detailed insights into the genetic background responsible for iron acquisition and menaquinone biosynthesis in anammox bacterial cells. Comparative analysis of the 'Ca. Scalindua' genomes revealed that the 1502 genes found in the 'Ca. S. japonica' genome were not present in the 'Ca. S. profunda' and 'Ca. S. rubra' genomes, showing a high genomic diversity. This result may reflect a high phylogenetic diversity of the genus 'Ca. Scalindua'.

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Media selection for anammox‐based polishing filters: Balancing anammox enrichment and retention with filtration function

Fofana

Peng

Huynh

et al. 2022

Water Environment Research

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Retrofitting conventional denitrification filters into partial denitrification‐anammox (PdNA)‐ or anammox (AnAOB)‐based filters will reduce the needs for external carbon addition. The success of AnAOB‐based filters depends on anammox growth and retention within such filters. Studies have overlooked the importance of media selection and its impact on AnAOB capacity, head loss progression dynamics, and shear conditions applied onto the AnAOB biofilm. The objective of this study was to evaluate viable media types (10 types) that can enhance AnAOB rates for efficient nitrogen removal in filters. Given the higher backwash requirement and lower AnAOB capacity of the conventionally used sand, expanded clay (3–5 mm) was recommended for AnAOB‐based filters in this study. Owing to its surface characteristics, expanded clay had higher AnAOB activity (304‐ vs. 104‐g NH4+‐N/m2/day) and higher AnAOB retention (43% more) than sand. Increasing the iron content of expanded clay to 37% resulted in an increase in zeta potential, which led to 56% more anammox capacity compared to expanded clay with 7% iron content. This work provides insight into the importance of media types in the growth and retention of AnAOB in filters, and this knowledge could be used as basis in the development of PdNA filters. Practitioner Points Expanded clay showed the lowest head loss buildup and most likely will result in longer runtime for full‐scale PdNA applications The highest AnAOB rates were achieved in expanded clay types and sand compared with smaller media typically used in biofiltration Expanded clay resulted in better AnAOB retention under shear, whereas sand could not withstand shear and required more frequent backwashing Expanded clay iron coating enhanced AnAOB enrichment and retention, most likely due to increased surface roughness and/or positive charge

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Iron assimilation and utilization in anaerobic ammonium oxidizing bacteria

Cited by 125 publications

References 61 publications

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

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

Genetic diversity of marine anaerobic ammonium‐oxidizing bacteria as revealed by genomic and proteomic analyses of ‘Candidatus Scalindua japonica’

Media selection for anammox‐based polishing filters: Balancing anammox enrichment and retention with filtration function

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