A 192-heme electron transfer network in the hydrazine dehydrogenase complex

Akram, Mohd; Dietl, Andreas; Mersdorf, Ulrike; Prinz, Simone; Maalcke, Wouter J.; Keltjens, Jan T.; Ferousi, Christina; Almeida, Naomi M. de; Reimann, Joachim; Kartal, Boran; Jetten, Mike S. M.; Parey, Kristian; Barends, Thomas R. M.

doi:10.1126/sciadv.aav4310

Cited by 50 publications

(67 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In contrast, many of the peptide replete cytochromes are catalytic and consist of dimeric or higher-order complexes, such as the 24 c-type heme HAO complex made of three octaheme cytochromes, 31 or the 192-heme hydrazine dehydratase complex made from 24 subunits each containing eight hemes. 32 The peptide minimized cytochromes have hemes aligned in pairs that are closely parallel or perpendicular; this allows for efficient electron transfer across the heme chain within the cytochrome. For these cytochromes there is a linear correlation between the number of hemes and the edge to edge length of the cytochrome ( Figure 5).…”

Section: Multiheme (4+) Cytochromesmentioning

confidence: 99%

“…The biologically relevant conformations of peptide minimized cytochromes are monomeric and proposed to be involved in electron transfer, electron scavenging, or electron storage. In contrast, many of the peptide replete cytochromes are catalytic and consist of dimeric or higher‐order complexes, such as the 24 c ‐type heme HAO complex made of three octaheme cytochromes, or the 192‐heme hydrazine dehydratase complex made from 24 subunits each containing eight hemes . The peptide minimized cytochromes have hemes aligned in pairs that are closely parallel or perpendicular; this allows for efficient electron transfer across the heme chain within the cytochrome.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

et al. 2019

View full text Add to dashboard Cite

Heme containing proteins are involved in a broad range of cellular functions, from oxygen sensing and transport to catalyzing oxidoreductive reactions. The two major types of cytochrome (b‐type and c‐type) only differ in their mechanism of heme attachment, but this has major implications for their cellular roles in both localization and mechanism. The b‐type cytochromes are commonly cytoplasmic, or are within the cytoplasmic membrane, while c‐type cytochromes are always found outside of the cytoplasm. The mechanism of heme attachment allows for complex c‐type multiheme complexes, having the capacity to hold multiple electrons, to be assembled. These are increasingly being identified as secreted into the extracellular environment. For organisms that respire using extracellular substrates, these large multiheme cytochromes allow for electron transfer networks from the cytoplasmic membrane to the cell exterior for the reduction of extracellular electron acceptors. In this review the structures and functions of these networks and the mechanisms by which electrons are transferred to extracellular substrates is described.

show abstract

Section: Multiheme (4+) Cytochromesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

et al. 2019

View full text Add to dashboard Cite

show abstract

“…4). The four low-potential electrons released from this reaction must be stored until they are transferred to a redox partner and feed the quinone (quinol) pool within the anammoxosome membrane to build up the membrane potential ( 80 ). Currently, it is not known how electrons are transported over membranes when NO 2 − is the electron acceptor.…”

Section: Supplementary Materialsmentioning

confidence: 99%

“…Understanding the electron flow and electron carriers is an important next step in anammox research. A recent exciting study showing the structure of the HDH ( 80 ), revealed that HDH can store up to 192 electrons and it is proposed that the appropriate carriers might specifically dock into the enzyme to get the electrons and transport them to the desired acceptor. This will prevent accidental transfer of the low-redox potential electrons to random acceptors.…”

Section: Supplementary Materialsmentioning

confidence: 99%

“…In the current proposed model of the anammox process, the four electrons released from the N 2 H 4 oxidation are transferred to the menaquinone pool in the anammoxosome membrane by the action of a yet unknown oxidoreductase ( 66, 80 ). The resulting proton gradient across the anammoxosome membrane drive the adenosine 5′-triphosphate (ATP) synthesis ( 80 ). However, in general, little is known about how anammox bacteria transport and utilize the energy released by the N 2 H 4 oxidation in the respiratory complexes in the anammoxosome membrane ( 80 ).…”

Section: Supplementary Materialsmentioning

confidence: 99%

See 1 more Smart Citation

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

Shaw

Ali

Katuri

et al. 2019

Preprint

View full text Add to dashboard Cite

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.

show abstract

Purification of the key enzyme complexes of the anammox pathway from DEMON sludge

et al. 2021

Self Cite

View full text Add to dashboard Cite

Anaerobic Ammonium Oxidation (“anammox”) is a bacterial process in which nitrite and ammonium are converted into nitrogen gas and water, yielding energy for the cell. Anammox is an important branch of the global biological nitrogen cycle, being responsible for up to 50% of the yearly nitrogen removal from the oceans. Strikingly, the anammox process uniquely relies on the extremely reactive and toxic compound hydrazine as a free intermediate. Given its global importance and biochemical novelty, there is considerable interest in the enzymes at the heart of the anammox pathway. Unfortunately, obtaining these enzymes in sufficiently large amounts for biochemical and structural studies is problematic, given the slow growth of pure cultures of anammox bacteria when high cell densities are required. However, the anammox process is being applied in wastewater treatment to remove nitrogenous waste in processes like DEamMONification (DEMON). In plants using such processes, which rely on a combination of aerobic ammonia‐oxidizers and anammox organisms, kilogram amounts of anammox bacteria‐containing sludge are readily available. Here, we report a protein isolation protocol starting from anammox cells present in DEMON sludge from a wastewater treatment plan that readily yields pure preparations of key anammox proteins in the tens of milligrams, including hydrazine synthase HZS and hydrazine dehydrogenase (HDH), as well as hydroxylamine oxidoreductase (HAO). HDH and HAO were active and of sufficient quality for biochemical studies and for HAO, the crystal structure could be determined. The method presented here provides a viable way to obtain materials for the study of proteins not only from the central anammox metabolism but also for the study of other exciting aspects of anammox bacteria, such as for example, their unusual ladderane lipids.

show abstract

A 192-heme electron transfer network in the hydrazine dehydrogenase complex

Cited by 50 publications

References 48 publications

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

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

Purification of the key enzyme complexes of the anammox pathway from DEMON sludge

Contact Info

Product

Resources

About