Discovery of a functional, contracted heme-binding motif within a multiheme cytochrome

Ferousi, Christina; Lindhoud, Simon; Baymann, Frauke; Hester, Eric R.; Reimann, Joachim; Kartal, Boran

doi:10.1074/jbc.ra119.010568

Cited by 27 publications

(17 citation statements)

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“…Under “normal” anammox conditions (i.e., NO 2 − as electron acceptor), the membrane associated quinol-interacting ETM encoded in the HZS gene cluster, mediate the first half-reaction for N 2 H 4 synthesis ( 66, 78 ). The ETM provides three-electrons to the HZS enzymatic complex for NO reduction to NH 2 OH with the help of an electron shuttle ( 78, 79 ). N 2 H 4 is further oxidized to N 2 by HDH (Fig.…”

Section: Supplementary Materialsmentioning

confidence: 99%

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%

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

Shaw

Ali

Katuri

et al. 2019

Preprint

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“…For example the octaheme MccA of Wollinella succinogenes includes a CX 15 CH heme binding site . Recently a “contracted” heme binding motif of CKCH was identified in a tetraheme protein that is part of the hydrazine synthase apparatus of annamox bacteria Kuenenia stuttgartiensis . However, it is clear that the adjacent cysteine‐histidine motif is critical, such that a similar motif CXXCK requires a separate ccm maturation system to covalently attach the heme to the active site of cytochrome c nitrite reductase NrfA.…”

Section: Introductionmentioning

confidence: 99%

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

et al. 2019

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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.

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“…The latter was recently characterized in detail and found to exchange electrons with HZS. 23 However, there is no a priori need for the redox partner of KsHAO to be a multiheme protein. As a typical trimeric HAO-like octaheme cytochrome c , KsHAO possesses a 24-heme electron relay system to transport electrons between the active site heme 4 of each monomer and electron-transfer sites on the surface of the protein.…”

Section: Discussionmentioning

confidence: 99%

Specificity of Small c-Type Cytochromes in Anaerobic Ammonium Oxidation

et al. 2021

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Anaerobic ammonium oxidation (anammox) is a bacterial process in which ammonium and nitrite are combined into dinitrogen gas and water, yielding energy for the cell. This process relies on a series of redox reactions catalyzed by a set of enzymes, with electrons being shuttled to and from these enzymes, likely by small cytochrome c proteins. For this system to work productively, these electron carriers require a degree of specificity toward the various possible redox partners they encounter in the cell. Here, we compare two cytochrome c proteins from the anammox model organism Kuenenia stuttgartiensis . We show that they are highly homologous, are expressed at comparable levels, share the same fold, and display highly similar redox potentials, yet one of them accepts electrons from the metabolic enzyme hydroxylamine oxidase (HAO) efficiently, whereas the other does not. An analysis of the crystal structures supplemented by Monte Carlo simulations of the transient redox interactions suggests that this difference is at least partly due to the electrostatic field surrounding the proteins, illustrating one way in which the electron carriers in anammox could attain the required specificity. Moreover, the simulations suggest a different “outlet” for electrons on HAO than has traditionally been assumed.

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Discovery of a functional, contracted heme-binding motif within a multiheme cytochrome

Cited by 27 publications

References 50 publications

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

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

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria

Specificity of Small c-Type Cytochromes in Anaerobic Ammonium Oxidation

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