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Stephen W Ragsdale - One of the best experts on this subject based on the ideXlab platform.
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crystallographic characterization of the carbonylated a cluster in carbon monoxide dehydrogenase acetyl coa synthase
ACS Catalysis, 2020Co-Authors: Steven E Cohen, Stephen W Ragsdale, Mehmet Can, Elizabeth C Wittenborn, Rachel A Hendrickson, Catherine L DrennanAbstract:The Wood–Ljungdahl Pathway allows for autotrophic bacterial growth on carbon dioxide, with the last step in acetyl-CoA synthesis catalyzed by the bifunctional enzyme carbon monoxide dehydrogenase/a...
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binding site for coenzyme a revealed in the structure of pyruvate ferredoxin oxidoreductase from moorella thermoacetica
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Percival Yangting Chen, Stephen W Ragsdale, Catherine L Drennan, Heather AmanAbstract:Pyruvate:ferredoxin oxidoreductase (PFOR) is a microbial enzyme that uses thiamine pyrophosphate (TPP), three [4Fe-4S] clusters, and coenzyme A (CoA) in the reversible oxidation of pyruvate to generate acetyl-CoA and carbon dioxide. The two electrons that are generated as a result of pyruvate decarboxylation are used in the reduction of low potential ferredoxins, which provide reducing equivalents for central metabolism, including the Wood–Ljungdahl Pathway. PFOR is a member of the 2-oxoacid:ferredoxin oxidoreductase (OFOR) superfamily, which plays major roles in both microbial redox reactions and carbon dioxide fixation. Here, we present a set of crystallographic snapshots of the best-studied member of this superfamily, the PFOR from Moorella thermoacetica ( Mt PFOR). These snapshots include the native structure, those of lactyl-TPP and acetyl-TPP reaction intermediates, and the first of an OFOR with CoA bound. These structural data reveal the binding site of CoA as domain III, the function of which in OFORs was previously unknown, and establish sequence motifs for CoA binding in the OFOR superfamily. Mt PFOR structures further show that domain III undergoes a conformational change upon CoA binding that seals off the active site and positions the thiolate of CoA directly adjacent to the TPP cofactor. These structural findings provide a molecular basis for the experimental observation that CoA binding accelerates catalysis by 10 5 -fold.
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one carbon chemistry of oxalate oxidoreductase captured by x ray crystallography
Proceedings of the National Academy of Sciences of the United States of America, 2016Co-Authors: Marcus I Gibson, Stephen W Ragsdale, Mehmet Can, Percival Yangting Chen, Elizabeth Pierce, Aileen C Johnson, Catherine L DrennanAbstract:Thiamine pyrophosphate (TPP)-dependent oxalate oxidoreductase (OOR) metabolizes oxalate, generating two molecules of CO 2 and two low-potential electrons, thus providing both the carbon and reducing equivalents for operation of the Wood−Ljungdahl Pathway of acetogenesis. Here we present structures of OOR in which two different reaction intermediate bound states have been trapped: the covalent adducts between TPP and oxalate and between TPP and CO 2 . These structures, along with the previously determined structure of substrate-free OOR, allow us to visualize how active site rearrangements can drive catalysis. Our results suggest that OOR operates via a bait-and-switch mechanism, attracting substrate into the active site through the presence of positively charged and polar residues, and then altering the electrostatic environment through loop and side chain movements to drive catalysis. This simple but elegant mechanism explains how oxalate, a molecule that humans and most animals cannot break down, can be used for growth by acetogenic bacteria.
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identification and characterization of oxalate oxidoreductase a novel thiamine pyrophosphate dependent 2 oxoacid oxidoreductase that enables anaerobic growth on oxalate
Journal of Biological Chemistry, 2010Co-Authors: Elizabeth Pierce, Donald F Becker, Stephen W RagsdaleAbstract:Abstract Moorella thermoacetica is an anaerobic acetogen, a class of bacteria that is found in the soil, the animal gastrointestinal tract, and the rumen. This organism engages the Wood-Ljungdahl Pathway of anaerobic CO2 fixation for heterotrophic or autotrophic growth. This paper describes a novel enzyme, oxalate oxidoreductase (OOR), that enables M. thermoacetica to grow on oxalate, which is produced in soil and is a common component of kidney stones. Exposure to oxalate leads to the induction of three proteins that are subunits of OOR, which oxidizes oxalate coupled to the production of two electrons and CO2 or bicarbonate. Like other members of the 2-oxoacid:ferredoxin oxidoreductase family, OOR contains thiamine pyrophosphate and three [Fe4S4] clusters. However, unlike previously characterized members of this family, OOR does not use coenzyme A as a substrate. Oxalate is oxidized with a kcat of 0.09 s−1 and a Km of 58 μm at pH 8. OOR also oxidizes a few other 2-oxoacids (which do not induce OOR) also without any requirement for CoA. The enzyme transfers its reducing equivalents to a broad range of electron acceptors, including ferredoxin and the nickel-dependent carbon monoxide dehydrogenase. In conjunction with the well characterized Wood-Ljungdahl Pathway, OOR should be sufficient for oxalate metabolism by M. thermoacetica, and it constitutes a novel Pathway for oxalate metabolism.
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infrared and epr spectroscopic characterization of a ni i species formed by photolysis of a catalytically competent ni i co intermediate in the acetyl coa synthase reaction
Biochemistry, 2010Co-Authors: Gunes Bender, Troy A Stich, Lifen Yan, David R Britt, Stephen P Cramer, Stephen W RagsdaleAbstract:Acetyl-CoA synthase (ACS) catalyzes the synthesis of acetyl-CoA from CO, coenzyme A (CoA), and a methyl group from the CH3-Co3+ site in the corrinoid iron−sulfur protein (CFeSP). These are the key steps in the Wood−Ljungdahl Pathway of anaerobic CO and CO2 fixation. The active site of ACS is the A-cluster, which is an unusual nickel−iron−sulfur cluster. There is significant evidence for the catalytic intermediacy of a CO-bound paramagnetic Ni species, with an electronic configuration of [Fe4S4]2+-(Nip+-CO)-(Nid2+), where Nip and Nid represent the Ni centers in the A-cluster that are proximal and distal to the [Fe4S4]2+ cluster, respectively. This well-characterized Nip+-CO intermediate is often called the NiFeC species. Photolysis of the Nip+-CO state generates a novel Nip+ species (Ared*) with a rhombic electron paramagnetic resonance spectrum (g values of 2.56, 2.10, and 2.01) and an extremely low (1 kJ/mol) barrier for recombination with CO. We suggest that the photolytically generated Ared* species is...
V Müller - One of the best experts on this subject based on the ideXlab platform.
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Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii
Environmental microbiology, 2018Co-Authors: Mats Lechtenfeld, Florian Kremp, Julia Heine, Janin Sameith, V MüllerAbstract:The quarternary, trimethylated amine glycine betaine (GB) is widespread in nature but its fate under anoxic conditions remains elusive. It can be used by some acetogenic bacteria as carbon and energy source but the Pathway of GB metabolism has not been elucidated. We have identified a gene cluster involved in GB metabolism and studied acetogenesis from GB in the model acetogen Acetobacterium woodii. GB is taken up by a secondary active, Na+ coupled transporter of the betaine-choline-carnitine (BCC) family. GB is demethylated to dimethylglycine, the end product of the reaction, by a methyltransferase system. Further conversion of the methyl group requires CO2 as well as Na+ indicating that GB metabolism involves the Wood-Ljungdahl Pathway. These studies culminate in a model for the path of carbon and electrons during acetogenensis from GB and a model for the bioenergetics of acetogenesis from GB.
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Ethylene glycol metabolism in the acetogen Acetobacterium woodii
Journal of bacteriology, 2016Co-Authors: Dragan Trifunović, Kai Schuchmann, V MüllerAbstract:ABSTRACT The acetogenic bacterium Acetobacterium woodii is able to grow by the oxidation of diols, such as 1,2-propanediol, 2,3-butanediol, or ethylene glycol. Recent analyses demonstrated fundamentally different ways for oxidation of 1,2-propanediol and 2,3-butanediol. Here, we analyzed the metabolism of ethylene glycol. Our data demonstrate that ethylene glycol is dehydrated to acetaldehyde, which is then disproportionated to ethanol and acetyl coenzyme A (acetyl-CoA). The latter is further converted to acetate, and this Pathway is coupled to ATP formation by substrate-level phosphorylation. Apparently, the product ethanol is in part further oxidized and the reducing equivalents are recycled by reduction of CO2 to acetate in the Wood-Ljungdahl Pathway. Biochemical data as well as the results of protein synthesis analysis are consistent with the hypothesis that the propane diol dehydratase (PduCDE) and CoA-dependent propionaldehyde dehydrogenase (PduP) proteins, encoded by the pdu gene cluster, also catalyze ethylene glycol dehydration to acetaldehyde and its CoA-dependent oxidation to acetyl-CoA. Moreover, genes encoding bacterial microcompartments as part of the pdu gene cluster are also expressed during growth on ethylene glycol, arguing for a dual function of the Pdu microcompartment system. IMPORTANCE Acetogenic bacteria are characterized by their ability to use CO2 as a terminal electron acceptor by a specific Pathway, the Wood-Ljungdahl Pathway, enabling in most acetogens chemolithoautotrophic growth with H2 and CO2. However, acetogens are very versatile and can use a wide variety of different substrates for growth. Here we report on the elucidation of the Pathway for utilization of ethylene glycol by the model acetogen Acetobacterium woodii. This diol is degraded by dehydration to acetaldehyde followed by a disproportionation to acetate and ethanol. We present evidence that this Pathway is catalyzed by the same enzyme system recently described for the utilization of 1,2-propanediol. The enzymes for ethylene glycol utilization seem to be encapsulated in protein compartments, known as bacterial microcompartments.
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A low phosphorylation potential in the acetogen Acetobacterium woodii reflects its lifestyle at the thermodynamic edge of life
Archives of Microbiology, 2015Co-Authors: Sebastian Spahn, Karsten Brandt, V MüllerAbstract:The anaerobic, acetogenic bacterium Acetobacterium woodii grows on hydrogen and carbon dioxide and uses the Wood–Ljungdahl Pathway to fix carbon but also to synthesize ATP. The free energy change of acetogenesis from H_2 + CO_2 allows for synthesis of only a fraction of an ATP under environmental conditions, and A. woodii is clearly a paradigm for microbial life under extreme energy limitation. However, it was unknown how much energy is required to make ATP under these conditions. In the present study, we determined the phosphorylation potential in cells metabolizing three different acetogenic substrates. It accounts to 37.9 ± 1.3 kJ/mol ATP during acetogenesis from fructose, 32.1 ± 0.3 kJ/mol ATP during acetogenesis from H_2 + CO_2 and 30.2 ± 0.9 kJ/mol ATP during acetogenesis from CO, the lowest phosphorylation potential ever described. The physiological consequences in terms of energy conservation under extreme energy limitation are discussed.
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2,3-Butanediol Metabolism in the Acetogen Acetobacterium woodii.
Applied and environmental microbiology, 2015Co-Authors: Verena Hess, Dragan Trifunović, Olga Oyrik, V MüllerAbstract:ABSTRACT The acetogenic bacterium Acetobacterium woodii is able to reduce CO2 to acetate via the Wood-Ljungdahl Pathway. Only recently we demonstrated that degradation of 1,2-propanediol by A. woodii was not dependent on acetogenesis, but that it is disproportionated to propanol and propionate. Here, we analyzed the metabolism of A. woodii on another diol, 2,3-butanediol. Experiments with growing and resting cells, metabolite analysis and enzymatic measurements revealed that 2,3-butanediol is oxidized in an NAD+-dependent manner to acetate via the intermediates acetoin, acetaldehyde, and acetyl coenzyme A. Ethanol was not detected as an end product, either in growing cultures or in cell suspensions. Apparently, all reducing equivalents originating from the oxidation of 2,3-butanediol were funneled into the Wood-Ljungdahl Pathway to reduce CO2 to another acetate. Thus, the metabolism of 2,3-butanediol requires the Wood-Ljungdahl Pathway.
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Nonacetogenic Growth of the Acetogen Acetobacterium woodii on 1,2-Propanediol
Journal of bacteriology, 2014Co-Authors: Kai Schuchmann, Silke Schmidt, Antonio Martinez Lopez, Christina Kaberline, Martin Kuhns, Wolfram Lorenzen, Helge B. Bode, Friederike Joos, V MüllerAbstract:Acetogenic bacteria can grow by the oxidation of various substrates coupled to the reduction of CO2 in the Wood-Ljungdahl Pathway. Here, we show that growth of the acetogen Acetobacterium woodii on 1,2-propanediol (1,2-PD) as the sole carbon and energy source is independent of acetogenesis. Enzymatic measurements and metabolite analysis revealed that 1,2-PD is dehydrated to propionaldehyde, which is further oxidized to propionyl coenzyme A (propionyl-CoA) with concomitant reduction of NAD. NADH is reoxidized by reducing propionaldehyde to propanol. The potential gene cluster coding for the responsible enzymes includes genes coding for shell proteins of bacterial microcompartments. Electron microscopy revealed the presence of microcompartments as well as storage granules in cells grown on 1,2-PD. Gene clusters coding for the 1,2-PD Pathway can be found in other acetogens as well, but the distribution shows no relation to the phylogeny of the organisms.
Catherine L Drennan - One of the best experts on this subject based on the ideXlab platform.
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crystallographic characterization of the carbonylated a cluster in carbon monoxide dehydrogenase acetyl coa synthase
ACS Catalysis, 2020Co-Authors: Steven E Cohen, Stephen W Ragsdale, Mehmet Can, Elizabeth C Wittenborn, Rachel A Hendrickson, Catherine L DrennanAbstract:The Wood–Ljungdahl Pathway allows for autotrophic bacterial growth on carbon dioxide, with the last step in acetyl-CoA synthesis catalyzed by the bifunctional enzyme carbon monoxide dehydrogenase/a...
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binding site for coenzyme a revealed in the structure of pyruvate ferredoxin oxidoreductase from moorella thermoacetica
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Percival Yangting Chen, Stephen W Ragsdale, Catherine L Drennan, Heather AmanAbstract:Pyruvate:ferredoxin oxidoreductase (PFOR) is a microbial enzyme that uses thiamine pyrophosphate (TPP), three [4Fe-4S] clusters, and coenzyme A (CoA) in the reversible oxidation of pyruvate to generate acetyl-CoA and carbon dioxide. The two electrons that are generated as a result of pyruvate decarboxylation are used in the reduction of low potential ferredoxins, which provide reducing equivalents for central metabolism, including the Wood–Ljungdahl Pathway. PFOR is a member of the 2-oxoacid:ferredoxin oxidoreductase (OFOR) superfamily, which plays major roles in both microbial redox reactions and carbon dioxide fixation. Here, we present a set of crystallographic snapshots of the best-studied member of this superfamily, the PFOR from Moorella thermoacetica ( Mt PFOR). These snapshots include the native structure, those of lactyl-TPP and acetyl-TPP reaction intermediates, and the first of an OFOR with CoA bound. These structural data reveal the binding site of CoA as domain III, the function of which in OFORs was previously unknown, and establish sequence motifs for CoA binding in the OFOR superfamily. Mt PFOR structures further show that domain III undergoes a conformational change upon CoA binding that seals off the active site and positions the thiolate of CoA directly adjacent to the TPP cofactor. These structural findings provide a molecular basis for the experimental observation that CoA binding accelerates catalysis by 10 5 -fold.
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one carbon chemistry of oxalate oxidoreductase captured by x ray crystallography
Proceedings of the National Academy of Sciences of the United States of America, 2016Co-Authors: Marcus I Gibson, Stephen W Ragsdale, Mehmet Can, Percival Yangting Chen, Elizabeth Pierce, Aileen C Johnson, Catherine L DrennanAbstract:Thiamine pyrophosphate (TPP)-dependent oxalate oxidoreductase (OOR) metabolizes oxalate, generating two molecules of CO 2 and two low-potential electrons, thus providing both the carbon and reducing equivalents for operation of the Wood−Ljungdahl Pathway of acetogenesis. Here we present structures of OOR in which two different reaction intermediate bound states have been trapped: the covalent adducts between TPP and oxalate and between TPP and CO 2 . These structures, along with the previously determined structure of substrate-free OOR, allow us to visualize how active site rearrangements can drive catalysis. Our results suggest that OOR operates via a bait-and-switch mechanism, attracting substrate into the active site through the presence of positively charged and polar residues, and then altering the electrostatic environment through loop and side chain movements to drive catalysis. This simple but elegant mechanism explains how oxalate, a molecule that humans and most animals cannot break down, can be used for growth by acetogenic bacteria.
Volker Muller - One of the best experts on this subject based on the ideXlab platform.
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genome scale analysis of acetobacterium woodii identifies translational regulation of acetogenesis
mSystems, 2021Co-Authors: Jongoh Shin, Yoseb Song, Volker Muller, Sangrak Jin, Seulgi Kang, Jungkul Lee, Dong Rip Kim, Suhyung Cho, Byungkwan ChoAbstract:Acetogens synthesize acetyl-CoA via the CO2-fixing Wood-Ljungdahl Pathway. Despite their ecological and biotechnological importance, their translational regulation of carbon and energy metabolisms remains unclear. Here, we report how carbon and energy metabolisms in the model acetogen Acetobacterium woodii are translationally controlled under different growth conditions. Data integration of genome-scale transcriptomic and translatomic analyses revealed that the acetogenesis genes, including those of the Wood-Ljungdahl Pathway and energy metabolism, showed changes in translational efficiency under autotrophic growth conditions. In particular, genes encoding the Wood-Ljungdahl Pathway are translated at similar levels to achieve efficient acetogenesis activity under autotrophic growth conditions, whereas genes encoding the carbonyl branch present increased translation levels in comparison to those for the methyl branch under heterotrophic growth conditions. The translation efficiency of genes in the Pathways is differentially regulated by 5' untranslated regions and ribosome-binding sequences under different growth conditions. Our findings provide potential strategies to optimize the metabolism of syngas-fermenting acetogenic bacteria for better productivity. IMPORTANCE Acetogens are capable of reducing CO2 to multicarbon compounds (e.g., ethanol or 2,3-butanediol) via the Wood-Ljungdahl Pathway. Given that protein synthesis in bacteria is highly energy consuming, acetogens living at the thermodynamic limit of life are inevitably under translation control. Here, we dissect the translational regulation of carbon and energy metabolisms in the model acetogen Acetobacterium woodii under heterotrophic and autotrophic growth conditions. The latter may be experienced when acetogen is used as a cell factory that synthesizes products from CO2 during the gas fermentation process. We found that the methyl and carbonyl branches of the Wood-Ljungdahl Pathway are activated at similar translation levels during autotrophic growth. Translation is mainly regulated by the 5'-untranslated-region structure and ribosome-binding-site sequence. This work reveals novel translational regulation for coping with autotrophic growth conditions and provides the systematic data set, including the transcriptome, translatome, and promoter/5'-untranslated-region bioparts.
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Adh4, an alcohol dehydrogenase controls alcohol formation within bacterial microcompartments in the acetogenic bacterium Acetobacterium woodii.
Environmental microbiology, 2020Co-Authors: Nilanjan Pal Chowdhury, Jimyung Moon, Volker MullerAbstract:Acetobacterium woodii utilizes the Wood-Ljungdahl Pathway for reductive synthesis of acetate from carbon dioxide. However, A. woodii can also perform non-acetogenic growth on 1,2-propanediol (1,2-PD) where instead of acetate, equal amounts of propionate and propanol are produced as metabolic end products. Metabolism of 1,2-PD occurs via encapsulated metabolic enzymes within large proteinaceous bodies called bacterial microcompartments. While the genome of A. woodii harbours 11 genes encoding putative alcohol dehydrogenases, the BMC-encapsulated propanol-generating alcohol dehydrogenase remains unidentified. Here, we show that Adh4 of A. woodii is the alcohol dehydrogenase required for propanol/ethanol formation within these microcompartments. It catalyses the NADH-dependent reduction of propionaldehyde or acetaldehyde to propanol or ethanol and primarily functions to recycle NADH within the BMC. Removal of adh4 gene from the A. woodii genome resulted in slow growth on 1,2-PD and the mutant displayed reduced propanol and enhanced propionate formation as a metabolic end product. In sum, the data suggest that Adh4 is responsible for propanol formation within the BMC and is involved in redox balancing in the acetogen, A. woodii.
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revealing formate production from carbon monoxide in wild type and mutants of rnf and ech containing acetogens acetobacterium woodii and thermoanaerobacter kivui
Microbial Biotechnology, 2020Co-Authors: Fabian M Schwarz, Anja Wiechmann, Sarah Ciurus, Surbhi Jain, Christoph Baum, Mirko Basen, Volker MullerAbstract:Acetogenic bacteria have gained much attraction in recent years as they can produce different biofuels and biochemicals from H2 plus CO2 or even CO alone, therefore opening a promising alternative route for the production of biofuels from renewable sources compared to existing sugar-based routes. However, CO metabolism still raises questions concerning the biochemistry and bioenergetics in many acetogens. In this study, we focused on the two acetogenic bacteria Acetobacterium woodii and Thermoanaerobacter kivui which, so far, are the only identified acetogens harbouring a H2 -dependent CO2 reductase and furthermore belong to different classes of 'Rnf'- and 'Ech-acetogens'. Both strains catalysed the conversion of CO into the bulk chemical acetate and formate. Formate production was stimulated by uncoupling the energy metabolism from the Wood-Ljungdahl Pathway, and specific rates of 1.44 and 1.34 mmol g-1 h-1 for A. woodii ∆rnf and T. kivui wild type were reached. The demonstrated CO-based formate production rates are, to the best of our knowledge, among the highest rates ever reported. Using mutants of ∆hdcr, ∆cooS, ∆hydBA, ∆rnf and ∆ech2 with deficiencies in key enzyme activities of the central metabolism enabled us to postulate two different CO utilization Pathways in these two model organisms.
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energetics and application of heterotrophy in acetogenic bacteria
Applied and Environmental Microbiology, 2016Co-Authors: Kai Schuchmann, Volker MullerAbstract:Acetogenic bacteria are a diverse group of strictly anaerobic bacteria that utilize the Wood-Ljungdahl Pathway for CO2 fixation and energy conservation. These microorganisms play an important part in the global carbon cycle and are a key component of the anaerobic food web. Their most prominent metabolic feature is autotrophic growth with molecular hydrogen and carbon dioxide as the substrates. However, most members also show an outstanding metabolic flexibility for utilizing a vast variety of different substrates. In contrast to autotrophic growth, which is hardly competitive, metabolic flexibility is seen as a key ability of acetogens to compete in ecosystems and might explain the almost-ubiquitous distribution of acetogenic bacteria in anoxic environments. This review covers the latest findings with respect to the heterotrophic metabolism of acetogenic bacteria, including utilization of carbohydrates, lactate, and different alcohols, especially in the model acetogen Acetobacterium woodii Modularity of metabolism, a key concept of Pathway design in synthetic biology, together with electron bifurcation, to overcome energetic barriers, appears to be the basis for the amazing substrate spectrum. At the same time, acetogens depend on only a relatively small number of enzymes to expand the substrate spectrum. We will discuss the energetic advantages of coupling CO2 reduction to fermentations that exploit otherwise-inaccessible substrates and the ecological advantages, as well as the biotechnological applications of the heterotrophic metabolism of acetogens.
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a bacterial hydrogen dependent co2 reductase forms filamentous structures
FEBS Journal, 2016Co-Authors: Kai Schuchmann, Janet Vonck, Volker MullerAbstract:Interconversion of CO2 and formic acid is an important reaction in bacteria. A novel enzyme complex that directly utilizes molecular hydrogen as electron donor for the reversible reduction of CO2 has recently been identified in the Wood-Ljungdahl Pathway of an acetogenic bacterium. This Pathway is utilized for carbon fixation as well as energy conservation. Here we describe the further characterization of the quaternary structure of this enzyme complex and the unexpected behavior of this enzyme in polymerizing into filamentous structures. Polymerization of metabolic enzymes into similar structures has been observed only in rare cases but the increasing number of examples point towards a more general characteristic of enzyme functioning. Polymerization of the purified enzyme into ordered filaments of more than 0.1 μm in length was only dependent on the presence of divalent cations. Polymerization was a reversible process and connected to the enzymatic activity of the oxygen-sensitive enzyme with the filamentous form being the most active state.
Zongze Shao - One of the best experts on this subject based on the ideXlab platform.
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"Candidatus Desulfobulbus rimicarensis," an Uncultivated Deltaproteobacterial Epibiont from the Deep-Sea Hydrothermal Vent Shrimp Rimicaris exoculata.
Applied and environmental microbiology, 2020Co-Authors: Lijing Jiang, Zhaobin Huang, Karine Alain, Xuewen Liu, Chunming Dong, Marie-anne Cambon-bonavita, Shasha Wang, Zongze ShaoAbstract:The deep-sea hydrothermal vent shrimp Rimicaris exoculata largely depends on a dense epibiotic chemoautotrophic bacterial community within its enlarged cephalothoracic chamber. However, our understanding of shrimp-bacterium interactions is limited. In this report, we focused on the deltaproteobacterial epibiont of R. exoculata from the relatively unexplored South Mid-Atlantic Ridge. A nearly complete genome of a Deltaproteobacteria epibiont was binned from the assembled metagenome. Whole-genome phylogenetic analysis reveals that it is affiliated with the genus Desulfobulbus, representing a potential novel species for which the name "Candidatus Desulfobulbus rimicarensis" is proposed. Genomic and transcriptomic analyses reveal that this bacterium utilizes the Wood-Ljungdahl Pathway for carbon assimilation and harvests energy via sulfur disproportionation, which is significantly different from other shrimp epibionts. Additionally, this epibiont has putative nitrogen fixation activity, but it is extremely active in directly taking up ammonia and urea from the host or vent environments. Moreover, the epibiont could be distinguished from its free-living relatives by various features, such as the lack of chemotaxis and motility traits, a dramatic reduction in biosynthesis genes for capsular and extracellular polysaccharides, enrichment of genes required for carbon fixation and sulfur metabolism, and resistance to environmental toxins. Our study highlights the unique role and symbiotic adaptation of Deltaproteobacteria in deep-sea hydrothermal vent shrimps.IMPORTANCE The shrimp Rimicaris exoculata represents the dominant faunal biomass at many deep-sea hydrothermal vent ecosystems along the Mid-Atlantic Ridge. This organism harbors dense bacterial epibiont communities in its enlarged cephalothoracic chamber that play an important nutritional role. Deltaproteobacteria are ubiquitous in epibiotic communities of R. exoculata, and their functional roles as epibionts are based solely on the presence of functional genes. Here, we describe "Candidatus Desulfobulbus rimicarensis," an uncultivated deltaproteobacterial epibiont. Compared to campylobacterial and gammaproteobacterial epibionts of R. exoculata, this bacterium possessed unique metabolic Pathways, such as the Wood-Ljungdahl Pathway, as well as sulfur disproportionation and nitrogen fixation Pathways. Furthermore, this epibiont can be distinguished from closely related free-living Desulfobulbus strains by its reduced genetic content and potential loss of functions, suggesting unique adaptations to the shrimp host. This study is a genomic and transcriptomic analysis of a deltaproteobacterial epibiont and largely expands the understanding of its metabolism and adaptation to the R. exoculata host.
