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

2019 ◽  
Author(s):  
Dario R. Shaw ◽  
Muhammad Ali ◽  
Krishna P. Katuri ◽  
Jeffrey A. Gralnick ◽  
Joachim Reimann ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Acceptor ◽  
Electron Acceptors ◽  
Extracellular Electron Transfer ◽  
Anammox Bacteria ◽  
Significant Finding ◽  
Ammonium Oxidation ◽  
Anaerobic Oxidation ◽  
Terminal Electron Acceptor ◽  
Carbon Based

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.

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

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Dario R. Shaw ◽  
Muhammad Ali ◽  
Krishna P. Katuri ◽  
Jeffrey A. Gralnick ◽  
Joachim Reimann ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Extracellular Electron Transfer ◽  
Anammox Bacteria ◽  
Anaerobic Oxidation

scholarly journals Cyclic Conversions in the Nitrogen Cycle

2021 ◽  
Vol 12 ◽  
Author(s):  
Robbert Kleerebezem ◽  
Sebastian Lücker
Keyword(s):  
Methane Oxidation ◽  
Electron Acceptor ◽  
Nitrogen Cycle ◽  
Inorganic Carbon ◽  
Carbon Fixation ◽  
Ammonia Oxidation ◽  
Anammox Bacteria ◽  
Ammonium Oxidation ◽  
Terminal Electron Acceptor

The cyclic nature of specific conversions in the nitrogen cycle imposes strict limitations to the conversions observed in nature and explains for example why anaerobic ammonium oxidation (anammox) bacteria can only use nitrite – and not nitrate – as electron acceptor in catabolism, and why nitrite is required as additional electron donor for inorganic carbon fixation in anabolism. Furthermore, the biochemistry involved in nitrite-dependent anaerobic methane oxidation excludes the feasibility of using nitrate as electron acceptor. Based on the cyclic nature of these nitrogen conversions, we propose two scenarios that may explain the ecological role of recently discovered complete ammonia-oxidizing (comammox) Nitrospira spp., some of which were initially found in a strongly oxygen limited environment: (i) comammox Nitrospira spp. may actually catalyze an anammox-like metabolism using a biochemistry similar to intra-oxic nitrite-dependent methane oxidation, or (ii) scavenge all available oxygen for ammonia activation and use nitrate as terminal electron acceptor. Both scenarios require the presence of the biochemical machinery for ammonia oxidation to nitrate, potentially explaining a specific ecological niche for the occurrence of comammox bacteria in nature.

scholarly journals Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake

2011 ◽  
Vol 77 (13) ◽  
pp. 4429-4436 ◽  
Author(s):  
Jörg S. Deutzmann ◽  
Bernhard Schink
Keyword(s):  
Methane Oxidation ◽  
Electron Acceptors ◽  
Molecular Techniques ◽  
Freshwater Lake ◽  
Lake Constance ◽  
Anaerobic Oxidation Of Methane ◽  
Anaerobic Oxidation ◽  
Terminal Electron Acceptor ◽  
Oxidation Of Methane ◽  
Freshwater Habitats

ABSTRACTAnaerobic oxidation of methane (AOM) with sulfate as terminal electron acceptor has been reported for various environments, including freshwater habitats, and also, nitrate and nitrite were recently shown to act as electron acceptors for methane oxidation in eutrophic freshwater habitats. Radiotracer experiments with sediment material of Lake Constance, an oligotrophic freshwater lake, were performed to follow14CO2formation from14CH4in sediment incubations in the presence of different electron acceptors, namely, nitrate, nitrite, sulfate, or oxygen. Whereas14CO2formation without and with sulfate addition was negligible, addition of nitrate increased14CO2formation significantly, suggesting that AOM could be coupled to denitrification. Nonetheless, denitrification-dependent AOM rates remained at least 1 order of magnitude lower than rates of aerobic methane oxidation. Using molecular techniques, putative denitrifying methanotrophs belonging to the NC10 phylum were detected on the basis of thepmoAand 16S rRNA gene sequences. These findings show that sulfate-dependent AOM was insignificant in Lake constant sediments. However, AOM can also be coupled to denitrification in this oligotrophic freshwater habitat, providing first indications that this might be a widespread process that plays an important role in mitigating methane emissions.

scholarly journals How thermophilic Gram-positive organisms perform extracellular electron transfer: characterization of the cell surface terminal reductase OcwA

2019 ◽  
Author(s):  
N.L. Costa ◽  
B. Hermann ◽  
V. Fourmond ◽  
M. Faustino ◽  
M. Teixeira ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Cell Surface ◽  
Electron Acceptors ◽  
Added Value ◽  
Extracellular Electron Transfer ◽  
Bioelectrochemical Systems ◽  
Positive Bacterium ◽  
Gram Positive ◽  
Evolutionary Pathway ◽  
Structural And Functional Properties

AbstractExtracellular electron transfer is the key process underpinning the development of bioelectrochemical systems for the production of energy or added-value compounds. Thermincola potens JR is a promising Gram-positive bacterium to be used in these systems because it is thermophilic. In this paper we describe the structural and functional properties of the nonaheme cytochrome OcwA, which is the terminal reductase of this organism. The structure of OcwA, determined at 2.2Å resolution shows that the overall-fold and organization of the hemes are not related to other metal reductases and instead are similar to that of multiheme cytochromes involved in the biogeochemical cycles of nitrogen and sulfur. We show that, in addition to solid electron acceptors, OcwA can also reduce soluble electron shuttles and oxyanions. These data reveal that OcwA can take the role of a respiratory ‘swiss-army knife’ allowing this organism to grow in environments with rapidly changing availability of terminal electron acceptors without the need for transcriptional regulation and protein synthesis.ImportanceThermophilic Gram-positive organisms were recently shown to be a promising class of organisms to be used in bioelectrochemical systems for the production of electrical energy. These organisms present a thick peptidoglycan layer that was thought to preclude them to perform extracellular electron transfer (i.e. exchange catabolic electrons with solid electron acceptors outside of the cell). In this manuscript we describe the structure and functional mechanisms of the multiheme cytochrome OcwA, the terminal reductase of the Gram-positive bacterium Thermincola potens JR found at the cell surface of this organism. The results presented here show that this protein is unrelated with terminal reductases found at the cell surface of other electroactive organisms. Instead, OcwA is similar to terminal reductases of soluble electron acceptors. Our data reveals that terminal oxidoreductases of soluble and insoluble substrates are evolutionarily related, providing novel insights into the evolutionary pathway of multiheme cytochromes.

scholarly journals Bacterial microcompartments linked to the flavin-based extracellular electron transfer drives anaerobic ethanolamine utilization in Listeria monocytogenes

2020 ◽  
Author(s):  
Zhe Zeng ◽  
Sjef Boeren ◽  
Varaang Bhandula ◽  
Samuel H. Light ◽  
Eddy J. Smid ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Listeria Monocytogenes ◽  
Electron Acceptor ◽  
Cell Membranes ◽  
Anaerobic Growth ◽  
Extracellular Electron Transfer ◽  
Severe Illness ◽  
Redox Imbalance ◽  
Bacterial Microcompartments

AbstractEthanolamine (EA) is a valuable microbial carbon and nitrogen source derived from phospholipids present in cell membranes. EA catabolism is suggested to occur in so-called bacterial microcompartments (BMCs) and activation of EA utilization (eut) genes is linked to bacterial pathogenesis. Despite reports showing that activation of eut in Listeria monocytogenes is regulated by a vitamin B12-binding riboswitch and that upregulation of eut genes occurs in mice, it remains unknown whether EA catabolism is BMC dependent. Here, we provide evidence for BMC-dependent anaerobic EA utilization via metabolic analysis, proteomics and electron microscopy. First, we show B12-induced activation of the eut operon in L. monocytogenes coupled to uptake and utilization of EA thereby enabling growth. Next, we demonstrate BMC formation in conjunction to EA catabolism with the production of acetate and ethanol in a molar ratio of 2:1. Flux via the ATP generating acetate branch causes an apparent redox imbalance due to reduced regeneration of NAD+ in the ethanol branch resulting in a surplus of NADH. We hypothesize that the redox imbalance is compensated by linking eut BMC to anaerobic flavin-based extracellular electron transfer (EET). Using L. monocytogenes wild type, a BMC mutant and a EET mutant, we demonstrate an interaction between BMC and EET and provide evidence for a role of Fe3+ as an electron acceptor. Taken together, our results suggest an important role of anaerobic BMC-dependent EA catabolism in the physiology of L. monocytogenes, with a crucial role for the flavin-based EET system in redox balancing.IMPORTANCEListeria monocytogenes is a food-borne pathogen causing severe illness and, as such, it is crucial to understand the molecular mechanisms contributing to pathogenicity. One carbon source that allows L. monocytogenes to grow in humans is ethanolamine (EA), which is derived from phospholipids present in eukaryotic cell membranes. It is hypothesized that EA utilization occurs in bacterial microcompartments (BMCs), self-assembling subcellular proteinaceous structures and analogs of eukaryotic organelles. Here, we demonstrate that BMC-driven utilization of EA in L. monocytogenes results in increased energy production essential for anaerobic growth. However, exploiting BMCs and the encapsulated metabolic pathways also requires balancing of oxidative and reductive pathways. We now provide evidence that L. monocytogenes copes with this by linking BMC activity to flavin-based extracellular electron transfer (EET) using iron as an electron acceptor. Our results shed new light on an important molecular mechanism that enables L. monocytogenes to grow using host-derived phospholipid degradation products.

scholarly journals Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors

mBio ◽  
2018 ◽  
Vol 9 (1) ◽  
Author(s):  
Annette R. Rowe ◽  
Pournami Rajeev ◽  
Abhiney Jain ◽  
Sahand Pirbadian ◽  
Akihiro Okamoto ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Complex I ◽  
Electron Transport Chain ◽  
Electron Flow ◽  
Extracellular Electron Transfer ◽  
Terminal Electron Acceptor ◽  
Cellular Energy ◽  
Transport Chain ◽  
Energy Acquisition

ABSTRACTWhile typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes,Shewanella oneidensisMR-1 can also facilitate electron flow from a cathode to terminal electron acceptors, such as fumarate or oxygen, thereby providing a model system for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain ofS. oneidensiswhen oxygen is used as the terminal electron acceptor. The effect of electron transport chain inhibitors suggested that a proton gradient is generated during cathode oxidation, consistent with the higher cellular ATP levels measured in cathode-respiring cells than in controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH2) pool determined with a bioluminescence assay, a proton uncoupler, and a mutant of proton-pumping NADH oxidase complex I. This work suggested that the generation of NADH/FMNH2under cathodic conditions was linked to reverse electron flow mediated by complex I. A decrease in cathodic electron uptake was observed in various mutant strains, including those lacking the extracellular electron transfer components necessary for anodic-current generation. While no cell growth was observed under these conditions, here we show that cathode oxidation is linked to cellular energy acquisition, resulting in a quantifiable reduction in the cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence on cathodes, which might extend to environments where growth and division are severely limited.IMPORTANCEThe majority of our knowledge of the physiology of extracellular electron transfer derives from studies of electrons moving to the exterior of the cell. The physiological mechanisms and/or consequences of the reverse processes are largely uncharacterized. This report demonstrates that when coupled to oxygen reduction, electrode oxidation can result in cellular energy acquisition. This respiratory process has potentially important implications for how microorganisms persist in energy-limited environments, such as reduced sediments under changing redox conditions. From an applied perspective, this work has important implications for microbially catalyzed processes on electrodes, particularly with regard to understanding models of cellular conversion of electrons from cathodes to microbially synthesized products.

scholarly journals Geothrix fermentans Secretes Two Different Redox-Active Compounds To Utilize Electron Acceptors across a Wide Range of Redox Potentials

2012 ◽  
Vol 78 (19) ◽  
pp. 6987-6995 ◽  
Author(s):  
Misha G. Mehta-Kolte ◽  
Daniel R. Bond
Keyword(s):  
Electron Transfer ◽  
Redox Potential ◽  
Electron Acceptor ◽  
Extracellular Electron Transfer ◽  
Redox Potentials ◽  
Active Compounds ◽  
Content Type ◽  
Electron Shuttles ◽  
Redox Active ◽  
Geothrix Fermentans

ABSTRACTThe current understanding of dissimilatory metal reduction is based primarily on isolates from the proteobacterial generaGeobacterandShewanella. However, environments undergoing active Fe(III) reduction often harbor less-well-studied phyla that are equally abundant. In this work, electrochemical techniques were used to analyze respiratory electron transfer by the only known Fe(III)-reducing representative of theAcidobacteria,Geothrix fermentans. In contrast to previously characterized metal-reducing bacteria, which typically reach maximal rates of respiration at electron acceptor potentials of 0 V versus standard hydrogen electrode (SHE),G. fermentansrequired potentials as high as 0.55 V to respire at its maximum rate. In addition,G. fermentanssecreted two different soluble redox-active electron shuttles with separate redox potentials (−0.2 V and 0.3 V). The compound with the lower midpoint potential, responsible for 20 to 30% of electron transfer activity, was riboflavin. The behavior of the higher-potential compound was consistent with hydrophilic UV-fluorescent molecules previously found inG. fermentanssupernatants. Both electron shuttles were also produced when cultures were grown with Fe(III), but not when fumarate was the electron acceptor. This study reveals thatGeothrixis able to take advantage of higher-redox-potential environments, demonstrates that secretion of flavin-based shuttles is not confined toShewanella, and points to the existence of high-potential-redox-active compounds involved in extracellular electron transfer. Based on differences between the respiratory strategies ofGeothrixandGeobacter, these two groups of bacteria could exist in distinctive environmental niches defined by redox potential.

scholarly journals Denitrification kinetics indicates nitrous oxide uptake is unaffected by electron competition in Accumulibacter

2020 ◽  
Author(s):  
Roy Samarpita ◽  
Pradhan Nirakar ◽  
NG How Yong ◽  
Wuertz Stefan
Keyword(s):  
Nitrous Oxide ◽  
Electron Acceptor ◽  
Phosphorus Removal ◽  
Metabolic Model ◽  
Electron Acceptors ◽  
Treatment Technology ◽  
Denitrifying Phosphorus Removal ◽  
Terminal Electron Acceptor ◽  
Efficient Treatment ◽  
Denitrification Kinetics

ABSTRACTDenitrifying phosphorus removal is a cost and energy efficient treatment technology that relies on polyphosphate accumulating organisms (DPAOs) utilizing nitrate or nitrite as terminal electron acceptor. Denitrification is a multistep process and many organisms do not possess the complete pathway, leading to the accumulation of intermediates such as nitrous oxide (N2O), a potent greenhouse gas and ozone depleting substance. Candidatus Accumulibacter organisms are prevalent in denitrifying phosphorus removal processes and, according to genomic analyses, appear to vary in their denitrification abilities based on their lineage. Yet, denitrification kinetics and nitrous oxide accumulation by Accumulibacter after long-term exposure to either nitrate or nitrite as electron acceptor have never been compared. We investigated the preferential use of the nitrogen oxides involved in denitrification and nitrous oxide accumulation in two enrichments of Accumulibacter and a competitor – the glycogen accumulating organism Candidatus Competibacter. A metabolic model was modified to predict phosphorus removal and denitrification rates when nitrate, nitrite or N2O were added as electron acceptors in different combinations. Unlike previous studies, no N2O accumulation was observed for Accumulibacter in the presence of multiple electron acceptors. Electron competition did not affect denitrification kinetics or N2O accumulation in Accumulibacter or Competibacter. Despite the presence of sufficient internal storage polymers (polyhydroxyalkanoates, or PHA) as energy source for each denitrification step, the extent of denitrification observed was dependent on the dominant organism in the enrichment. Accumulibacter showed complete denitrification and N2O utilization, whereas for Competibacter denitrification was limited to reduction of nitrate to nitrite. These findings indicate that DPAOs can contribute to lowering N2O emissions in the presence of multiple electron acceptors under partial nitritation conditions.

scholarly journals Escherichia coli cytochrome c peroxidase is a respiratory oxidase that enables the use of hydrogen peroxide as a terminal electron acceptor

2017 ◽  
Vol 114 (33) ◽  
pp. E6922-E6931 ◽  
Author(s):  
Maryam Khademian ◽  
James A. Imlay
Keyword(s):  
Escherichia Coli ◽  
Hydrogen Peroxide ◽  
Carbon Source ◽  
Electron Acceptor ◽  
Electron Acceptors ◽  
Flux Rate ◽  
Terminal Electron Acceptor ◽  
E Coli ◽  
Nonfermentable Carbon Source ◽  
Quinone Pool

Microbial cytochrome c peroxidases (Ccp) have been studied for 75 years, but their physiological roles are unclear. Ccps are located in the periplasms of bacteria and the mitochondrial intermembrane spaces of fungi. In this study, Ccp is demonstrated to be a significant degrader of hydrogen peroxide in anoxic Escherichia coli. Intriguingly, ccp transcription requires both the presence of H2O2 and the absence of O2. Experiments show that Ccp lacks enough activity to shield the cytoplasm from exogenous H2O2. However, it receives electrons from the quinone pool, and its flux rate approximates flow to other anaerobic electron acceptors. Indeed, Ccp enabled E. coli to grow on a nonfermentable carbon source when H2O2 was supplied. Salmonella behaved similarly. This role rationalizes ccp repression in oxic environments. We speculate that micromolar H2O2 is created both biologically and abiotically at natural oxic/anoxic interfaces. The OxyR response appears to exploit this H2O2 as a terminal oxidant while simultaneously defending the cell against its toxicity.

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