Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation
TL;DR: Four flavin-containing cytoplasmatic multienzyme complexes from anaerobic bacteria and archaea that catalyze the reduction of the low potential ferredoxin by electron donors with higher potentials at ≤ 100 kPa are described.
About: This article is published in Biochimica et Biophysica Acta.The article was published on 2013-02-01 and is currently open access. It has received 633 citations till now. The article focuses on the topics: Ferredoxin & Hydrogenase.
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Pacific Northwest National Laboratory1, California Institute of Technology2, Princeton University3, Humboldt University of Berlin4, Pennsylvania State University5, Brookhaven National Laboratory6, University of California, Riverside7, University of Illinois at Urbana–Champaign8, United States Department of Energy9, University of California, Berkeley10, University of Toronto11, University of Michigan12, University of Amsterdam13, Utah State University14, Max Planck Society15, Louisiana State University16
TL;DR: Providing a future energy supply that is secure and CO_2-neutral will require switching to nonfossil energy sources such as wind, solar, nuclear, and geothermal energy and developing methods for transforming the energy produced by these new sources into forms that can be stored, transported, and used upon demand.
Abstract: Two major energy-related problems confront the world in the
next 50 years. First, increased worldwide competition for
gradually depleting fossil fuel reserves (derived from past
photosynthesis) will lead to higher costs, both monetarily and politically. Second, atmospheric CO_2 levels are at their highest recorded level since records began. Further increases are predicted to produce large and uncontrollable impacts on the world climate. These projected impacts extend beyond climate to ocean acidification, because the ocean is a major sink for atmospheric CO2.1 Providing a future energy supply that is secure and CO_2-neutral will require switching to nonfossil energy sources such as wind, solar, nuclear, and geothermal energy and developing methods for transforming the energy produced by these new sources into forms that can be stored, transported, and used upon demand.
1,651 citations
TL;DR: This overview emphasizes the important role played by cross-feeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria.
Abstract: The human gut microbiota ferments dietary non-digestible carbohydrates into short-chain fatty acids (SCFA). These microbial products are utilized by the host and propionate and butyrate in particular exert a range of health-promoting functions. Here an overview of the metabolic pathways utilized by gut microbes to produce these two SCFA from dietary carbohydrates and from amino acids resulting from protein breakdown is provided. This overview emphasizes the important role played by cross-feeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria. The ecophysiology, including growth requirements and responses to environmental factors, of major propionate and butyrate producing bacteria are discussed in relation to dietary modulation of these metabolites. A detailed understanding of SCFA metabolism by the gut microbiota is necessary to underpin effective strategies to optimize SCFA supply to the host.
1,379 citations
Cites background from "Energy conservation via electron bi..."
...4A, which also assumes that some of the reducing power that is generated drives proton export, increasing the ATP yield per glucose fermented (Buckel & Thauer, 2013)....
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TL;DR: The data support the theory of an autotrophic origin of life involving the Wood–Ljungdahl pathway in a hydrothermal setting and identify clostridia and methanogens, whose modern lifestyles resemble that of LUCA, as basal among their respective domains.
Abstract: The concept of a last universal common ancestor of all cells (LUCA, or the progenote) is central to the study of early evolution and life's origin, yet information about how and where LUCA lived is lacking. We investigated all clusters and phylogenetic trees for 6.1 million protein coding genes from sequenced prokaryotic genomes in order to reconstruct the microbial ecology of LUCA. Among 286,514 protein clusters, we identified 355 protein families (∼0.1%) that trace to LUCA by phylogenetic criteria. Because these proteins are not universally distributed, they can shed light on LUCA's physiology. Their functions, properties and prosthetic groups depict LUCA as anaerobic, CO2-fixing, H2-dependent with a Wood-Ljungdahl pathway, N2-fixing and thermophilic. LUCA's biochemistry was replete with FeS clusters and radical reaction mechanisms. Its cofactors reveal dependence upon transition metals, flavins, S-adenosyl methionine, coenzyme A, ferredoxin, molybdopterin, corrins and selenium. Its genetic code required nucleoside modifications and S-adenosyl methionine-dependent methylations. The 355 phylogenies identify clostridia and methanogens, whose modern lifestyles resemble that of LUCA, as basal among their respective domains. LUCA inhabited a geochemically active environment rich in H2, CO2 and iron. The data support the theory of an autotrophic origin of life involving the Wood-Ljungdahl pathway in a hydrothermal setting.
692 citations
TL;DR: The principles of classical and non-classical syntrophy are explained and biochemical fundamentals that allow microorganism to survive under a range of environmental conditions and to drive important biogeochemical processes are presented.
Abstract: Classical definitions of syntrophy focus on a process, performed through metabolic interaction between dependent microbial partners, such as the degradation of complex organic compounds under anoxic conditions. However, examples from past and current scientific discoveries suggest that a new, simple but wider definition is necessary to cover all aspects of microbial syntrophy. We suggest the term ‘obligately mutualistic metabolism’, which still focuses on microbial metabolic cooperation but also includes an ecological aspect: the benefit for both partners. By the combined metabolic activity of microorganisms, endergonic reactions can become exergonic through the efficient removal of products and therefore enable a microbial community to survive with minimal energy resources. Here, we explain the principles of classical and non-classical syntrophy and illustrate the concepts with various examples. We present biochemical fundamentals that allow microorganism to survive under a range of environmental conditions and to drive important biogeochemical processes. Novel technologies have contributed to the understanding of syntrophic relationships in cultured and uncultured systems. Recent research highlights that obligately mutualistic metabolism is not limited to certain metabolic pathways nor to certain environments or microorganisms. This beneficial microbial interaction is not restricted to the transfer of reducing agents such as hydrogen or formate, but can also involve the exchange of organic, sulfurous- and nitrogenous compounds or the removal of toxic compounds.
628 citations
Cites background from "Energy conservation via electron bi..."
...…with anaerobic fatty acid oxidation (through CoA intermediates), once the C-H bond is activated (Heider, 2007), and insights into anaerobic aliphatic and aromatic acid metabolism will also facilitate a better understanding of hydrocarbon oxidation by syntrophic communities in the coming years....
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...The multienzyme cytoplasmic complexes that catalyze these reactions couple endergonic and exergonic redox reactions through the simultaneous oxidation of the ferredoxin electron donor with a higher potential acceptor (Buckel & Thauer, 2013)....
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TL;DR: The latest progress on the biochemistry and genetics of the energy metabolism of model acetogens are discussed, elucidating how these bacteria couple CO2 fixation to energy conservation.
Abstract: Life on earth evolved in the absence of oxygen with inorganic gases as potential sources of carbon and energy. Among the alternative mechanisms for carbon dioxide (CO₂) fixation in the living world, only the reduction of CO₂ by the Wood-Ljungdahl pathway, which is used by acetogenic bacteria, complies with the two requirements to sustain life: conservation of energy and production of biomass. However, how energy is conserved in acetogenic bacteria has been an enigma since their discovery. In this Review, we discuss the latest progress on the biochemistry and genetics of the energy metabolism of model acetogens, elucidating how these bacteria couple CO₂ fixation to energy conservation.
590 citations
References
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TL;DR: This article corrects the article on p. 100 in vol.
Abstract: [This corrects the article on p. 100 in vol. 41.].
3,345 citations
TL;DR: A three-dimensional structure for the monomeric iron-containing hydrogenase (CpI) from Clostridium pasteurianum was determined, providing insights into the mechanism of biological hydrogen activation and has broader implications for [Fe-S] cluster structure and function in biological systems.
Abstract: A three-dimensional structure for the monomeric iron-containing hydrogenase (CpI) from Clostridium pasteurianum was determined to 1.8 angstrom resolution by x-ray crystallography using multiwavelength anomalous dispersion (MAD) phasing. CpI, an enzyme that catalyzes the two-electron reduction of two protons to yield dihydrogen, was found to contain 20 gram atoms of iron per mole of protein, arranged into five distinct [Fe-S] clusters. The probable active-site cluster, previously termed the H-cluster, was found to be an unexpected arrangement of six iron atoms existing as a [4Fe-4S] cubane subcluster covalently bridged by a cysteinate thiol to a [2Fe] subcluster. The iron atoms of the [2Fe] subcluster both exist with an octahedral coordination geometry and are bridged to each other by three non-protein atoms, assigned as two sulfide atoms and one carbonyl or cyanide molecule. This structure provides insights into the mechanism of biological hydrogen activation and has broader implications for [Fe-S] cluster structure and function in biological systems.
1,719 citations
TL;DR: The data and analyses presented here highlight the ability to identify organizing metabolic principles from systems-level absolute metabolite concentration data, and facilitate efficient flux reversibility given thermodynamic and osmotic constraints.
Abstract: Absolute metabolite concentrations are critical to a quantitative understanding of cellular metabolism, as concentrations impact both the free energies and rates of metabolic reactions. Here we use LC-MS/MS to quantify more than 100 metabolite concentrations in aerobic, exponentially growing Escherichia coli with glucose, glycerol or acetate as the carbon source. The total observed intracellular metabolite pool was approximately 300 mM. A small number of metabolites dominate the metabolome on a molar basis, with glutamate being the most abundant. Metabolite concentration exceeds K(m) for most substrate-enzyme pairs. An exception is lower glycolysis, where concentrations of intermediates are near the K(m) of their consuming enzymes and all reactions are near equilibrium. This may facilitate efficient flux reversibility given thermodynamic and osmotic constraints. The data and analyses presented here highlight the ability to identify organizing metabolic principles from systems-level absolute metabolite concentration data.
1,631 citations
"Energy conservation via electron bi..." refers background in this paper
...Ferredoxin (Fd, clostridial type) [4,5] Fd+e−=Fd− Fd−+e−=Fd2− NAD [6] NAD+2 e−+H+=NADH NADP [6] NADP+2 e−+H+=NADPH...
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...For the understanding of the thermodynamics of Reactions (1) to (4) it is important to know that in living cells ferredoxins are generally more than 90% reduced (E'=−500 mV), that NAD is more than 90% oxidized (E'=−280 mV) and that the NADP/NADPH ratio is 1/40 (E'=−360 mV) [6]....
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TL;DR: In methanogens with cytochromes, the first and last steps in methanogenesis from CO2 are coupled chemiosmotically, whereas in methenogens without cyto Chromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.
Abstract: Most methanogenic archaea can reduce CO(2) with H(2) to methane, and it is generally assumed that the reactions and mechanisms of energy conservation that are involved are largely the same in all methanogens. However, this does not take into account the fact that methanogens with cytochromes have considerably higher growth yields and threshold concentrations for H(2) than methanogens without cytochromes. These and other differences can be explained by the proposal outlined in this Review that in methanogens with cytochromes, the first and last steps in methanogenesis from CO(2) are coupled chemiosmotically, whereas in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.
1,620 citations
"Energy conservation via electron bi..." refers background or methods in this paper
...Also used were E'=−320 mV for the NAD/NADH couple, E'=−320 mV for the NADP/NADPH couple, E'=−10 mV for the crotonyl-CoA/butyryl-CoA couple [10] and E'=–140 mV for the CoM-S-S-CoB/CoM-SH+CoB-SH couple (Table 1) [29]....
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...Thus transhydrogenation from NADH (E'=−280 mV) to NADP (E'=−360 mV) in living cells requires energy [30] as does the reduction of ferredoxin (E'=−500 mV) with H2 at 10 Pa (E'=−300 mV), which is the H2 partial pressure in methanogenic habitats [29]....
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...In Methanosarcina barkeri and in Archaeoglobus fulgidus the mvhD gene is fused to the 3′-end of hdrA [29,53]....
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...It has been proposed that in these hydrogenotrophic methanogens the F420 reducing hydrogenase FrhAG rather than MvhAG forms a functional electron bifurcating complex [29]....
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...2) replenishes the reduced ferredoxin required for the anabolic reduction of CO2 to pyruvate which involves a ferredoxin-dependent reduction of CO2 to CO (E'=−520 mV) and a ferredoxin-dependent reduction of acetylCoA+CO2 to pyruvate (E'=−500 mV) [29,53]....
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TL;DR: An overview of the nitrogenase system is presented in this article that emphasizes the structural organization of the proteins and associated metalloclusters that have the remarkable ability to catalyse nitrogen fixation under ambient conditions.
Abstract: Biological nitrogen fixation is mediated by the nitrogenase enzyme system that catalyses the ATP dependent reduction of atmospheric dinitrogen to ammonia. Nitrogenase consists of two component metalloproteins, the MoFe-protein with the FeMo-cofactor that provides the active site for substrate reduction, and the Fe-protein that couples ATP hydrolysis to electron transfer. An overview of the nitrogenase system is presented that emphasizes the structural organization of the proteins and associated metalloclusters that have the remarkable ability to catalyse nitrogen fixation under ambient conditions. Although the mechanism of ammonia formation by nitrogenase remains enigmatic, mechanistic inferences motivated by recent developments in the areas of nitrogenase biochemistry, spectroscopy, model chemistry and computational studies are discussed within this structural framework.
982 citations