Acetogens utilize the acetyl-CoA Wood-Ljungdahl pathway as a terminal electron-accepting, energy-conserving, CO(2)-fixing process. The decades of research to resolve the enzymology of this pathway (1) preceded studies demonstrating that acetogens not only harbor a novel CO(2)-fixing pathway, but are also ecologically important, and (2) overshadowed the novel microbiological discoveries of acetogens and acetogenesis. The first acetogen to be isolated, Clostridium aceticum, was reported by Klaas Tammo Wieringa in 1936, but was subsequently lost. The second acetogen to be isolated, Clostridium thermoaceticum, was isolated by Francis Ephraim Fontaine and co-workers in 1942. C. thermoaceticum became the most extensively studied acetogen and was used to resolve the enzymology of the acetyl-CoA pathway in the laboratories of Harland Goff Wood and Lars Gerhard Ljungdahl. Although acetogenesis initially intrigued few scientists, this novel process fostered several scientific milestones, including the first (14)C-tracer studies in biology and the discovery that tungsten is a biologically active metal. The acetyl-CoA pathway is now recognized as a fundamental component of the global carbon cycle and essential to the metabolic potentials of many different prokaryotes. The acetyl-CoA pathway and variants thereof appear to be important to primary production in certain habitats and may have been the first autotrophic process on earth and important to the evolution of life. The purpose of this article is to (1) pay tribute to those who discovered acetogens and acetogenesis, and to those who resolved the acetyl-CoA pathway, and (2) highlight the ecology and physiology of acetogens within the framework of their scientific roots.
The gut of the earthworm constitutes a mobile anoxic microzone to which the microorganisms of aerated soils are subjected. During gut passage, the in situ factors of the earthworm gut, which include anoxia and high concentrations of organic substrates, appear to greatly stimulate a subset of ingested soil microorganisms, including denitrifying and fermentative bacteria. The selective stimulation of ingested soil microbes by the unique microconditions of the earthworm gut (a) results in the in vivo emission of denitrification-derived dinitrogen (N(2)) and the greenhouse gas nitrous oxide (N(2)O) by the earthworm, and (b) might affect the fitness, culturability, and diversity of certain members of soil microbial biomes. These observations illustrate the impact that soil macrofauna might have on terrestrial nitrogen cycle processes via their transient hosting of ingested prokaryotes.
The emission of methane (1.3 mmol of CH 4 m ؊2 day ؊1 ), precursors of methanogenesis, and the methanogenic microorganisms of acidic bog peat (pH 4.4) from a moderately reduced forest site were investigated by in situ measurements, microcosm incubations, and cultivation methods, respectively. Bog peat produced CH 4 (0.4 to 1.7 mol g [dry wt] of soil ؊1 day ؊1 ) under anoxic conditions. At in situ pH, supplemental H 2 -CO 2 , ethanol, and 1-propanol all increased CH 4 production rates while formate, acetate, propionate, and butyrate inhibited the production of CH 4 ; methanol had no effect. H 2 -dependent acetogenesis occurred in H 2 -CO 2 -supplemented bog peat only after extended incubation periods. Nonsupplemented bog peat initially produced small amounts of H 2 that were subsequently consumed. The accumulation of H 2 was stimulated by ethanol and 1-propanol or by inhibiting methanogenesis with bromoethanesulfonate, and the consumption of ethanol was inhibited by large amounts of H 2 ; these results collectively indicated that ethanol-or 1-propanol-utilizing bacteria were trophically associated with H 2 -utilizing methanogens. A total of 10 9 anaerobes and 10 7 hydrogenotrophic methanogens per g (dry weight) of bog peat were enumerated by cultivation techniques. A stable methanogenic enrichment was obtained with an acidic, H 2 -CO 2 -supplemented, fatty acid-enriched defined medium. CH 4 production rates by the enrichment were similar at pH 4.5 and 6.5, and acetate inhibited methanogenesis at pH 4.5 but not at pH 6.5. A total of 27 different archaeal 16S rRNA gene sequences indicative of Methanobacteriaceae, Methanomicrobiales, and Methanosarcinaceae were retrieved from the highest CH 4 -positive serial dilutions of bog peat and methanogenic enrichments. A total of 10 bacterial 16S rRNA gene sequences were also retrieved from the same dilutions and enrichments and were indicative of bacteria that might be responsible for the production of H 2 that could be used by hydrogenotrophic methanogens. These results indicated that in this acidic bog peat, (i) H 2 is an important substrate for acid-tolerant methanogens, (ii) interspecies hydrogen transfer is involved in the degradation of organic carbon, (iii) the accumulation of protonated volatile fatty acids inhibits methanogenesis, and (iv) methanogenesis might be due to the activities of methanogens that are phylogenetic members of the Methanobacteriaceae, Methanomicrobiales, and Methanosarcinaceae.
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Low-sulfate, acidic (approximately pH 4) fens in the Lehstenbach catchment in the Fichtelgebirge mountains in Germany are unusual habitats for sulfate-reducing prokaryotes (SRPs) that have been postulated to facilitate the retention of sulfur and protons in these ecosystems. Despite the low in situ availability of sulfate (concentration in the soil solution, 20 to 200 M) and the acidic conditions (soil and soil solution pHs, approximately 4 and 5, respectively), the upper peat layers of the soils from two fens (Schlöppnerbrunnen I and II) of this catchment displayed significant sulfate-reducing capacities. 16S rRNA gene-based oligonucleotide microarray analyses revealed stable diversity patterns for recognized SRPs in the upper 30 cm of both fens. Members of the family "Syntrophobacteraceae" were detected in both fens, while signals specific for the genus Desulfomonile were observed only in soils from Schlöppnerbrunnen I. These results were confirmed and extended by comparative analyses of environmentally retrieved 16S rRNA and dissimilatory (bi)sulfite reductase (dsrAB) gene sequences; dsrAB sequences from Desulfobacca-like SRPs, which were not identified by microarray analysis, were obtained from both fens. Hypotheses concerning the ecophysiological role of these three SRP groups in the fens were formulated based on the known physiological properties of their cultured relatives. In addition to these recognized SRP lineages, six novel dsrAB types that were phylogenetically unrelated to all known SRPs were detected in the fens. These dsrAB sequences had no features indicative of pseudogenes and likely represent novel, deeply branching, sulfate-or sulfite-reducing prokaryotes that are specialized colonists of low-sulfate habitats.The dissimilatory reduction of sulfate is carried out exclusively by prokaryotic organisms and is one of the most important mineralization processes in anoxic aquatic environments, especially marine sediments (29,30). In contrast to well-studied sulfate-reducing communities in marine (18,19,38,41,53,56,57,72) and freshwater habitats (39,40,59,60), relatively little is known about the distribution, diversity, and in situ activities of sulfate-reducing prokaryotes (SRPs) in terrestrial ecosystems. The contribution of terrestrial SRPs to the overall turnover of organic matter is likely of minor importance on a global scale. However, SRPs contribute to the biodegradation of pollutants in soils and subsurface environments (1,15,49,71) and are important to the geomicrobiology of specialized terrestrial habitats that are subject to flooding, such as rice fields (68,76,77) and fens (3,5). ␦ 34 S values and 35 S-labeling patterns indicate that the dissimilatory reduction of sulfate is an ongoing process in the acidic fens of a forested catchment in northern Bavaria, Germany (Lehstenbach, Fichtelgebirge) (3, 5). The deposition of sulfur that originated from the combustion of soft coal in Eastern Europe (10) led to accumulation of sulfur in the soils of this catchment (4). Although pollution contro...
The in vivo production of nitrous oxide (N 2 O) by earthworms is due to their gut microbiota, and it is hypothesized that the microenvironment of the gut activates ingested N 2 O-producing soil bacteria. In situ measurement of N 2 O and O 2 with microsensors demonstrated that the earthworm gut is anoxic and the site of N 2 O production. The gut had a pH of 6.9 and an average water content of approximately 50%. The water content within the gut decreased from the anterior end to the posterior end. In contrast, the concentration of N 2 O increased from the anterior end to the mid-gut region and then decreased along the posterior part of the gut. Compared to the soil in which worms lived and fed, the gut of the earthworm was highly enriched in total carbon, organic carbon, and total nitrogen and had a C/N ratio of 7 (compared to a C/N ratio of 12 in soil). The aqueous phase of gut contents contained up to 80 mM glucose and numerous compounds that were indicative of anaerobic metabolism, including up to 9 mM formate, 8 mM acetate, 3 mM lactate, and 2 mM succinate. Compared to the soil contents, nitrite and ammonium were enriched in the gut up to 10-and 100-fold, respectively. The production of N 2 O by soil was induced when the gut environment was simulated in anoxic microcosms for 24 h (the approximate time for passage of soil through the earthworm). Anoxia, high osmolarity, nitrite, and nitrate were the dominant factors that stimulated the production of N 2 O. Supplemental organic carbon had a very minimal stimulatory effect on the production of N 2 O, and addition of buffer or ammonium had essentially no effect on the initial N 2 O production rates. However, a combination of supplements yielded rates greater than that obtained mathematically for single supplements, suggesting that the maximum rates observed were due to synergistic effects of supplements. Collectively, these results indicate that the special microenvironment of the earthworm gut is ideally suited for N 2 O-producing bacteria and support the hypothesis that the in situ conditions of the earthworm gut activate ingested N 2 O-producing soil bacteria during gut passage.Denitrification in the earthworm gut is involved in the in vivo emission of N 2 O by earthworms (23), cultured denitrifiers occur in high numbers in the earthworm gut (17), and denitrification can occur in earthworm casts (9, 35). Most denitrifiers possess the capacity to both produce and consume N 2 O (6), and the net release of N 2 O during denitrification is regulated by various parameters, including pH (29), the phase of growth (3), and the concentrations of nitrate and electron donors (19). High numbers of other organisms that are capable of producing N 2 O (i.e., nitrate-dissimilating and nitrifying bacteria) are also present in the earthworm gut (14). Production of N 2 O by nitrate-dissimilating bacteria is favored in systems that contain high levels of organic carbon, like the rumen or the gastrointestinal tracts of higher animals (18, 36). Some nitrifiers are able to use nitrate...
Strains of Clostidum thermoaceticum were tested for H2-and CO-dependent growth in a defined medium containing metals, minerals, vitamins, cysteine-sulfide, C02-bicarbonate, and H2 or CO. Ten of the thirteen strains tested grew at the expense of H2 and CO, and C. thermoaceticum ATCC 39073 was chosen for further study. The doubling times for H2-and CO-dependent growth under chemolithotrophic conditiods (the defined medium with nicotinic acid as sole essential vitamin and sulfide as sole reducer) were 25 and 10 h, respectively.Product stoichiometries for chemolithotrophic cultures approximated: 4.1H2 + 2.4CO2-+CH3COOH + 0.1 cell C + 0.3 unrecovered C and 6.8CO-*CH3COOH + 3.5CO2 + 0.4 cell C + 0.9 unrecovered C. H2-dependent growth produced signifiantly higher acetate concentrations per unit of biomass synthesized than did CO-or glucose-dependent growth. In dated the minimal nutritional requirements of this acetogen (37) so that a definitive assessment could be made of its heterotrophic and chemolithotrophic potentials. In the study presented here, numerous strains of C. thermoaceticum were obtained from various sources and evaluated. In addition, Acetogenium kivui (33, 34), a thermophilic nonclostridial acetogen which is capable of H2-dependent chemolithotrophic growth, was also included in this evaluation and used for comparative purposes. In this report, we demonstrate for the first time that certain strains of C. thermoaceticum grow chemolithotrophically (requiring only trace levels of nicotinic acid as the sole vitamin) at the expense of H2 or CO. Besides the overall metabolic properties exhibited by C. thermoaceticum and A. kivui under chemolithotrophic conditions, evidence is also presented which suggests that the type of energy source used during growth (e.g., H2 versus glucose) influences the expression or activity of hydrogenase and CO dehydrogenase in both of these acetogens. MATERIALS AND METHODSBacterial strains and cultivation. C. thermoaceticum (see Table 1 for strains used in this study) and A.
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