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Andreas Brune - One of the best experts on this subject based on the ideXlab platform.
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metabolic potential for reductive Acetogenesis and a novel energy converting nife hydrogenase in bathyarchaeia from termite guts a genome centric analysis
Frontiers in Microbiology, 2021Co-Authors: Hui Qi Loh, Vincent Herve, Andreas BruneAbstract:Symbiotic digestion of lignocellulose in the hindgut of higher termites is mediated by a diverse assemblage of bacteria and archaea. During a large-scale metagenomic study, we reconstructed 15 metagenome-assembled genomes (MAGs) of Bathyarchaeia that represent two distinct lineages in subgroup 6 (formerly MCG-6) unique to termite guts. One lineage (TB2; Candidatus Termitimicrobium) encodes all enzymes required for reductive Acetogenesis from CO2 via an archaeal variant of the Wood–Ljungdahl pathway, involving tetrahydromethanopterin as C1 carrier and an (ADP-forming) acetyl-CoA synthase. This includes a novel 11-subunit hydrogenase, which possesses the genomic architecture of the respiratory Fpo-complex of other archaea but whose catalytic subunit is phylogenetically related to and shares the conserved [NiFe] cofactor-binding motif with [NiFe] hydrogenases of subgroup 4g. We propose that this novel Fpo-like hydrogenase provides part of the reduced ferredoxin required for CO2 reduction and is driven by the electrochemical membrane potential generated from the ATP conserved by substrate-level phosphorylation; the other part may require the oxidation of organic electron donors, which would make members of TB2 mixotrophic acetogens. Members of the other lineage (TB1; Candidatus Termiticorpusculum) are definitely organotrophic because they consistently lack hydrogenases and/or methylene-tetrahydromethanopterin reductase, a key enzyme of the archaeal Wood–Ljungdahl pathway. Both lineages have the genomic capacity to reduce ferredoxin by oxidizing amino acids and might conduct methylotrophic Acetogenesis using unidentified methylated compound(s). Our results indicate that Bathyarchaeia of subgroup 6 contribute to acetate formation in the guts of higher termites and substantiate the genomic evidence for reductive Acetogenesis from organic substrates, possibly including methylated compounds, in other uncultured representatives of the phylum.
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metabolic potential for reductive Acetogenesis and a novel energy converting nife hydrogenase in bathyarchaeia from termite guts a genome centric analysis
bioRxiv, 2020Co-Authors: Hui Qi Loh, Vincent Herve, Andreas BruneAbstract:Abstract Symbiotic digestion of lignocellulose in the hindgut of higher termites is mediated by a diverse assemblage of bacteria and archaea. During a large-scale metagenomic study, we reconstructed 15 metagenome-assembled genomes (MAGs) of Bathyarchaeia that represent two distinct lineages in subgroup 6 (formerly MCG-6) unique to termite guts. One lineage (TB2; Candidatus Termitimicrobium) encodes all enzymes required for reductive Acetogenesis from H2 and CO2 via an archaeal variant of the Wood–Ljungdahl pathway. This includes a novel 11-subunit hydrogenase, which possesses the genomic architecture of the respiratory Fpo-complex of other archaea but whose catalytic subunit is phylogenetically related to and shares the conserved [NiFe] cofactor-binding motif with [NiFe] hydrogenases of subgroup 4g. We propose that this novel Fpo-like hydrogenase provides the reduced ferredoxin required for CO2 reduction and is driven by the electrochemical membrane potential generated from the ATP conserved by substrate-level phosphorylation. Members of the other lineage (TB1; Candidatus Termiticorpusculum) are not capable of lithotrophic Acetogenesis because they consistently lack hydrogenases and/or methylene-tetrahydromethanopterin reductase, a key enzyme of the pathway. Both lineages have the genomic capacity to reduce ferredoxin by oxidizing amino acids and might conduct methylotrophic Acetogenesis using unidentified methylated compound(s). Our results indicate that Bathyarchaeia of subgroup 6 contribute to acetate formation in the guts of higher termites and substantiate the genomic evidence for reductive Acetogenesis from organic substrates, including methylated compounds, in other uncultured representatives of the phylum.
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localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil feeding higher termites cubitermes spp
Applied and Environmental Microbiology, 1999Co-Authors: Anne Tholen, Andreas BruneAbstract:Methanogenesis and homoAcetogenesis occur simultaneously in the hindguts of almost all termites, but the reasons for the apparent predominance of methanogenesis over homoAcetogenesis in the hindgut of the humivorous species is not known. We found that in gut homogenates of soil-feeding Cubitermes spp., methanogens outcompete homoacetogens for endogenous reductant. The rates of methanogenesis were always significantly higher than those of reductive Acetogenesis, whereas the stimulation of Acetogenesis by the addition of exogenous H2 or formate was more pronounced than that of methanogenesis. In a companion paper, we reported that the anterior gut regions of Cubitermes spp. accumulated hydrogen to high partial pressures, whereas H2 was always below the detection limit (<100 Pa) in the posterior hindgut, and that all hindgut compartments turned into efficient H2 sinks when external H2 was provided (D. Schmitt-Wagner and A. Brune, Appl. Environ. Microbiol. 65:4490–4496, 1999). Using a microinjection technique, we found that only the posterior gut sections P3/4a and P4b, which harbored methanogenic activities, formed labeled acetate from H14CO3−. Enumeration of methanogenic and homoacetogenic populations in the different gut sections confirmed the coexistence of both metabolic groups in the same compartments. However, the in situ rates of Acetogenesis were strongly hydrogen limited; in the P4b section, no activity was detected unless external H2 was added. Endogenous rates of reductive Acetogenesis in isolated guts were about 10-fold lower than the in vivo rates of methanogenesis, but were almost equal when exogenous H2 was supplied. We conclude that the homoacetogenic populations in the posterior hindgut are supported by either substrates other than H2 or by a cross-epithelial H2 transfer from the anterior gut regions, which may create microniches favorable for H2-dependent Acetogenesis.
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hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil feeding higher termites cubitermes spp
Applied and Environmental Microbiology, 1999Co-Authors: Dirk Schmittwagner, Andreas BruneAbstract:It has been shown that the coexistence of methanogenesis and reductive Acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes is based largely on the radial distribution of the respective microbial populations and relatively high hydrogen partial pressures in the gut lumen. Using Clark-type microelectrodes, we showed that the situation in Cubitermes orthognathus and other soil-feeding members of the subfamily Termitinae is different and much more complex. All major compartments of agarose-embedded hindguts were anoxic at the gut center, and high H2 partial pressures (1 to 10 kPa) in the alkaline anterior region rendered the mixed segment and the third proctodeal segment (P3) significant sources of H2. Posterior to the P3 segment, however, H2 concentrations were generally below the detection limit (<100 Pa). All hindgut compartments turned into efficient hydrogen sinks when external H2 was supplied, but methane was formed mainly in the P3/4a and P4b compartments, and in the latter only when H2 or formate was added. Addition of H2 to the gas headspace stimulated CH4 emission of living termites, indicating that endogenous H2 production limits methanogenesis also in vivo. At the low H2 partial pressures in the posterior hindgut, methanogens would most likely outcompete homoacetogens for this electron donor. This might explain the apparent predominance of methanogenesis over reductive Acetogenesis in the hindgut of soil-feeding termites, although the presence of homoacetogens in the anterior, highly alkaline region cannot yet be excluded. In addition, the direct contact of anterior and posterior hindgut compartments in situ permits a cross-epithelial transfer of H2 or formate, which would not only fuel methanogenesis in these compartments, but would also create favorable microniches for reductive Acetogenesis. In situ rates and spatial distribution of H2-dependent acetogenic activities are addressed in a companion paper (A. Tholen and A. Brune, Appl. Environ. Microbiol. 65:4497‐4505, 1999). In the metabolic reactions involved in lignocellulose degradation in termite hindguts, hydrogen appears to be the key intermediate linking the fermentative breakdown of carbohydrates with methanogenesis and reductive Acetogenesis. In lower termites, H2 formation is mainly attributed to the dense populations of cellulolytic flagellates which are characteristic for this group. In higher termites, symbiotic flagellates are absent, and the reactions responsible for the formation of H2 are not known. Reductive Acetogenesis and methanogenesis, however, occur in all termites investigated to date and are considered typical for the strictly anaerobic metabolic activities in termite guts (for reviews, see references 9‐11).
Mark C M Van Loosdrecht - One of the best experts on this subject based on the ideXlab platform.
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candidatus galacturonibacter soehngenii shows acetogenic catabolism of galacturonic acid but lacks a canonical carbon monoxide dehydrogenase acetyl coa synthase complex
Frontiers in Microbiology, 2020Co-Authors: Laura C Valk, Martijn Diender, Gerben R Stouten, Jette Fischer Petersen, Per Halkjaer Nielsen, Morten Simonsen Dueholm, Jack T Pronk, Mark C M Van LoosdrechtAbstract:Acetogens have the ability to fixate carbon during fermentation by employing the Wood-Ljungdahl pathway (WLP), which is highly conserved across Bacteria and Archaea. In a previous study, product stoichometries in galacturonate-limited, anaerobic enrichment cultures of "Candidatus Galacturonibacter soehngenii," from a novel genus within the Lachnospiraceae, suggested the simultaneous operation of a modified Entner-Doudoroff pathway for galacturonate fermentation and a WLP for Acetogenesis. However, a draft metagenome-assembled genome (MAG) based on short reads did not reveal homologs of genes encoding a canonical WLP carbon-monoxide-dehydrogenase/acetyl-Coenzyme A synthase (CODH/ACS) complex. In this study, NaH13CO3 fed to chemostat-grown, galacturonate-limited enrichment cultures of "Ca. G. soehngenii" was shown to be incorporated into acetate. Preferential labeling of the carboxyl group of acetate was consistent with Acetogenesis via a WLP in which the methyl group of acetate was predominately derived from formate. This interpretation was further supported by high transcript levels of a putative pyruvate-formate lyase gene and very low transcript levels of a candidate gene for formate dehydrogenase. Reassembly of the "Ca. G. soehngenii" MAG with support from long-read nanopore sequencing data produced a single-scaffold MAG, which confirmed the absence of canonical CODH/ACS-complex genes homologs. However, high CO-dehydrogenase activities were measured in cell extracts of "Ca. G. soehngenii" enrichment cultures, contradicting the absence of corresponding homologs in the MAG. Based on the highly conserved amino-acid motif associated with anaerobic Ni-CO dehydrogenase proteins, a novel candidate was identified which could be responsible for the observed activities. These results demonstrate operation of an acetogenic pathway, most probably as a yet unresolved variant of the Wood-Ljungdahl pathway, in anaerobic, galacturonate-limited cultures of "Ca. G. soehngenii."
Stephen W Ragsdale - One of the best experts on this subject based on the ideXlab platform.
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Acetogenesis and the wood ljungdahl pathway of co2 fixation
Biochimica et Biophysica Acta, 2008Co-Authors: Stephen W Ragsdale, Elizabeth PierceAbstract:Conceptually, the simplest way to synthesize an organic molecule is to construct it one carbon at a time. The Wood-Ljungdahl pathway of CO(2) fixation involves this type of stepwise process. The biochemical events that underlie the condensation of two one-carbon units to form the two-carbon compound, acetate, have intrigued chemists, biochemists, and microbiologists for many decades. We begin this review with a description of the biology of Acetogenesis. Then, we provide a short history of the important discoveries that have led to the identification of the key components and steps of this usual mechanism of CO and CO(2) fixation. In this historical perspective, we have included reflections that hopefully will sketch the landscape of the controversies, hypotheses, and opinions that led to the key experiments and discoveries. We then describe the properties of the genes and enzymes involved in the pathway and conclude with a section describing some major questions that remain unanswered.
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enzymology of the wood ljungdahl pathway of Acetogenesis
Annals of the New York Academy of Sciences, 2008Co-Authors: Stephen W RagsdaleAbstract:The biochemistry of Acetogenesis is reviewed. The microbes that catalyze the reactions that are central to Acetogenesis are described and the focus is on the enzymology of the process. These microbes play a key role in the global carbon cycle, producing over 10 trillion kilograms of acetic acid annually. Acetogens have the ability to anaerobically convert carbon dioxide and CO into acetyl-CoA by the Wood-Ljungdahl pathway, which is linked to energy conservation. They also can convert the six carbons of glucose stoichiometrically into 3 mol of acetate using this pathway. Acetogens and other anaerobic microbes (e.g., sulfate reducers and methanogens) use the Wood-Ljungdahl pathway for cell carbon synthesis. Important enzymes in this pathway that are covered in this review are pyruvate ferredoxin oxidoreductase, CO dehydrogenase/acetyl-CoA synthase, a corrinoid iron-sulfur protein, a methyltransferase, and the enzymes involved in the conversion of carbon dioxide to methyl-tetrahydrofolate.
Martijn Diender - One of the best experts on this subject based on the ideXlab platform.
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candidatus galacturonibacter soehngenii shows acetogenic catabolism of galacturonic acid but lacks a canonical carbon monoxide dehydrogenase acetyl coa synthase complex
Frontiers in Microbiology, 2020Co-Authors: Laura C Valk, Martijn Diender, Gerben R Stouten, Jette Fischer Petersen, Per Halkjaer Nielsen, Morten Simonsen Dueholm, Jack T Pronk, Mark C M Van LoosdrechtAbstract:Acetogens have the ability to fixate carbon during fermentation by employing the Wood-Ljungdahl pathway (WLP), which is highly conserved across Bacteria and Archaea. In a previous study, product stoichometries in galacturonate-limited, anaerobic enrichment cultures of "Candidatus Galacturonibacter soehngenii," from a novel genus within the Lachnospiraceae, suggested the simultaneous operation of a modified Entner-Doudoroff pathway for galacturonate fermentation and a WLP for Acetogenesis. However, a draft metagenome-assembled genome (MAG) based on short reads did not reveal homologs of genes encoding a canonical WLP carbon-monoxide-dehydrogenase/acetyl-Coenzyme A synthase (CODH/ACS) complex. In this study, NaH13CO3 fed to chemostat-grown, galacturonate-limited enrichment cultures of "Ca. G. soehngenii" was shown to be incorporated into acetate. Preferential labeling of the carboxyl group of acetate was consistent with Acetogenesis via a WLP in which the methyl group of acetate was predominately derived from formate. This interpretation was further supported by high transcript levels of a putative pyruvate-formate lyase gene and very low transcript levels of a candidate gene for formate dehydrogenase. Reassembly of the "Ca. G. soehngenii" MAG with support from long-read nanopore sequencing data produced a single-scaffold MAG, which confirmed the absence of canonical CODH/ACS-complex genes homologs. However, high CO-dehydrogenase activities were measured in cell extracts of "Ca. G. soehngenii" enrichment cultures, contradicting the absence of corresponding homologs in the MAG. Based on the highly conserved amino-acid motif associated with anaerobic Ni-CO dehydrogenase proteins, a novel candidate was identified which could be responsible for the observed activities. These results demonstrate operation of an acetogenic pathway, most probably as a yet unresolved variant of the Wood-Ljungdahl pathway, in anaerobic, galacturonate-limited cultures of "Ca. G. soehngenii."
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pathways and bioenergetics of anaerobic carbon monoxide fermentation
Frontiers in Microbiology, 2015Co-Authors: Martijn Diender, Alfons J M Stams, D Z SousaAbstract:Carbon monoxide can act as a substrate for different modes of fermentative anaerobic metabolism. The trait of utilizing CO is spread among a diverse group of microorganisms, including members of bacteria as well as archaea. Over the last decade this metabolism has gained interest due to the potential of converting CO-rich gas, such as synthesis gas, into bio-based products. Three main types of fermentative CO metabolism can be distinguished: hydrogenogenesis, methanogenesis, and Acetogenesis, generating hydrogen, methane and acetate, respectively. Here, we review the current knowledge on these three variants of microbial CO metabolism with an emphasis on the potential enzymatic routes and bio-energetics involved.
Laura C Valk - One of the best experts on this subject based on the ideXlab platform.
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candidatus galacturonibacter soehngenii shows acetogenic catabolism of galacturonic acid but lacks a canonical carbon monoxide dehydrogenase acetyl coa synthase complex
Frontiers in Microbiology, 2020Co-Authors: Laura C Valk, Martijn Diender, Gerben R Stouten, Jette Fischer Petersen, Per Halkjaer Nielsen, Morten Simonsen Dueholm, Jack T Pronk, Mark C M Van LoosdrechtAbstract:Acetogens have the ability to fixate carbon during fermentation by employing the Wood-Ljungdahl pathway (WLP), which is highly conserved across Bacteria and Archaea. In a previous study, product stoichometries in galacturonate-limited, anaerobic enrichment cultures of "Candidatus Galacturonibacter soehngenii," from a novel genus within the Lachnospiraceae, suggested the simultaneous operation of a modified Entner-Doudoroff pathway for galacturonate fermentation and a WLP for Acetogenesis. However, a draft metagenome-assembled genome (MAG) based on short reads did not reveal homologs of genes encoding a canonical WLP carbon-monoxide-dehydrogenase/acetyl-Coenzyme A synthase (CODH/ACS) complex. In this study, NaH13CO3 fed to chemostat-grown, galacturonate-limited enrichment cultures of "Ca. G. soehngenii" was shown to be incorporated into acetate. Preferential labeling of the carboxyl group of acetate was consistent with Acetogenesis via a WLP in which the methyl group of acetate was predominately derived from formate. This interpretation was further supported by high transcript levels of a putative pyruvate-formate lyase gene and very low transcript levels of a candidate gene for formate dehydrogenase. Reassembly of the "Ca. G. soehngenii" MAG with support from long-read nanopore sequencing data produced a single-scaffold MAG, which confirmed the absence of canonical CODH/ACS-complex genes homologs. However, high CO-dehydrogenase activities were measured in cell extracts of "Ca. G. soehngenii" enrichment cultures, contradicting the absence of corresponding homologs in the MAG. Based on the highly conserved amino-acid motif associated with anaerobic Ni-CO dehydrogenase proteins, a novel candidate was identified which could be responsible for the observed activities. These results demonstrate operation of an acetogenic pathway, most probably as a yet unresolved variant of the Wood-Ljungdahl pathway, in anaerobic, galacturonate-limited cultures of "Ca. G. soehngenii."
