Anaerobic Oxidation of Toluene, Phenol, and p-Cresol by the Dissimilatory Iron-Reducing Organism, GS-15
01 Jun 1990-Applied and Environmental Microbiology (American Society for Microbiology)-Vol. 56, Iss: 6, pp 1858-1864
TL;DR: The metabolism of toluene, phenol, and p-cresol by GS-15 provides a model for how aromatic hydrocarbons and phenols may be oxidized with the reduction of Fe(III) in contaminated aquifers and petroleum-containing sediments.
Abstract: The dissimilatory Fe(III) reducer, GS-15, is the first microorganism known to couple the oxidation of aromatic compounds to the reduction of Fe(III) and the first example of a pure culture of any kind known to anaerobically oxidize an aromatic hydrocarbon, toluene. In this study, the metabolism of toluene, phenol, and p-cresol by GS-15 was investigated in more detail. GS-15 grew in an anaerobic medium with toluene as the sole electron donor and Fe(III) oxide as the electron acceptor. Growth coincided with Fe(III) reduction. [ring-14C]toluene was oxidized to 14CO2, and the stoichiometry of 14CO2 production and Fe(III) reduction indicated that GS-15 completely oxidized toluene to carbon dioxide with Fe(III) as the electron acceptor. Magnetite was the primary iron end product during toluene oxidation. Phenol and p-cresol were also completely oxidized to carbon dioxide with Fe(III) as the sole electron acceptor, and GS-15 could obtain energy to support growth by oxidizing either of these compounds as the sole electron donor. p-Hydroxybenzoate was a transitory extracellular intermediate of phenol and p-cresol metabolism but not of toluene metabolism. GS-15 oxidized potential aromatic intermediates in the oxidation of toluene (benzylalcohol and benzaldehyde) and p-cresol (p-hydroxybenzylalcohol and p-hydroxybenzaldehyde). The metabolism described here provides a model for how aromatic hydrocarbons and phenols may be oxidized with the reduction of Fe(III) in contaminated aquifers and petroleum-containing sediments. Images
Citations
More filters
TL;DR: The physiological characteristics of Geobacter species appear to explain why they have consistently been found to be the predominant Fe(III)- and Mn(IV)-reducing microorganisms in a variety of sedimentary environments.
2,633 citations
TL;DR: The physiological responses of microorganisms to the presence of hydrocarbons, including cell surface alterations and adaptive mechanisms for uptake and efflux of these substrates, have been characterized and used to investigate the dynamics of microbial communities in petroleum-impacted ecosystems.
Abstract: Recent advances in molecular biology have extended our understanding of the metabolic processes related to microbial transformation of petroleum hydrocarbons. The physiological responses of microorganisms to the presence of hydrocarbons, including cell surface alterations and adaptive mechanisms for uptake and efflux of these substrates, have been characterized. New molecular techniques have enhanced our ability to investigate the dynamics of microbial communities in petroleum-impacted ecosystems. By establishing conditions which maximize rates and extents of microbial growth, hydrocarbon access, and transformation, highly accelerated and bioreactor-based petroleum waste degradation processes have been implemented. Biofilters capable of removing and biodegrading volatile petroleum contaminants in air streams with short substrate-microbe contact times ( 2 S and sulfoxides from petrochemical waste streams. Microbes also have potential for use in removal of nitrogen from crude oil leading to reduced nitric oxide emissions provided that technical problems similar to those experienced in biodesulfurization can be solved. Enzymes are being exploited to produce added-value products from petroleum substrates, and bacterial biosensors are being used to analyze petroleum-contaminated environments.
1,346 citations
TL;DR: In this article, dissimilatory Fe(III)-reducing microorganisms can obtain energy for growth by electron transport to U(VI), which can be much faster than commonly cited abiological mechanisms for reduction.
Abstract: REDUCTION of the soluble, oxidized form of uranium, U(VI), to insoluble U(IV) is an important mechanism for the immobilization of uranium in aquatic sediments and for the formation of some uranium ores1–10. U(VI) reduction has generally been regarded as an abiological reaction in which sulphide, molecular hydrogen or organic compounds function as the reductant1,2,5,11. Microbial involvement in U(VI) reduction has been considered to be limited to indirect effects, such as microbial metabolism providing the reduced compounds for abiological U(VI) reduction and microbial cell walls providing a surface to stimulate abiological U(VI) reduction1,12,13. We report here, however, that dissimilatory Fe(III)-reducing microorganisms can obtain energy for growth by electron transport to U(VI). This novel form of microbial metabolism can be much faster than commonly cited abiological mechanisms for U(VI) reduction. Not only do these findings expand the known potential terminal electron acceptors for microbial energy transduction, they offer a likely explanation for the deposition of uranium in aquatic sediments and aquifers, and suggest a method for biological remediation of environments contaminated with uranium.
1,322 citations
TL;DR: The ability to oxidize hydrogen with the reduction of Fe(III) is a highly conserved characteristic of hyperthermophilic microorganisms, most notably those in the Geobacteraceae family as mentioned in this paper.
Abstract: Dissimilatory Fe(III) and Mn(IV) reduction has an important influence on the geochemistry of modern environments, and Fe(III)-reducing microorganisms, most notably those in the Geobacteraceae family, can play an important role in the bioremediation of subsurface environments contaminated with organic or metal contaminants. Microorganisms with the capacity to conserve energy from Fe(III) and Mn(IV) reduction are phylogenetically dispersed throughout the Bacteria and Archaea. The ability to oxidize hydrogen with the reduction of Fe(III) is a highly conserved characteristic of hyperthermophilic microorganisms and one Fe(III)-reducing Archaea grows at the highest temperature yet recorded for any organism. Fe(III)- and Mn(IV)-reducing microorganisms have the ability to oxidize a wide variety of organic compounds, often completely to carbon dioxide. Typical alternative electron acceptors for Fe(III) reducers include oxygen, nitrate, U(VI) and electrodes. Unlike other commonly considered electron acceptors, Fe(III) and Mn(IV) oxides, the most prevalent form of Fe(III) and Mn(IV) in most environments, are insoluble. Thus, Fe(III)- and Mn(IV)-reducing microorganisms face the dilemma of how to transfer electrons derived from central metabolism onto an insoluble, extracellular electron acceptor. Although microbiological and geochemical evidence suggests that Fe(III) reduction may have been the first form of microbial respiration, the capacity for Fe(III) reduction appears to have evolved several times as phylogenetically distinct Fe(III) reducers have different mechanisms for Fe(III) reduction. Geobacter species, which are representative of the family of Fe(III) reducers that predominate in a wide diversity of sedimentary environments, require direct contact with Fe(III) oxides in order to reduce them. In contrast, Shewanella and Geothrix species produce chelators that solubilize Fe(III) and release electron-shuttling compounds that transfer electrons from the cell surface to the surface of Fe(III) oxides not in direct contact with the cells. Electron transfer from the inner membrane to the outer membrane in Geobacter and Shewanella species appears to involve an electron transport chain of inner-membrane, periplasmic, and outer-membrane c-type cytochromes, but the cytochromes involved in these processes in the two organisms are different. In addition, Geobacter species specifically express flagella and pili during growth on Fe(III) and Mn(IV) oxides and are chemotactic to Fe(II) and Mn(II), which may lead Geobacter species to the oxides under anoxic conditions. The physiological characteristics of Geobacter species appear to explain why they have consistently been found to be the predominant Fe(III)- and Mn(IV)-reducing microorganisms in a variety of sedimentary environments. In comparison with other respiratory processes, the study of Fe(III) and Mn(IV) reduction is in its infancy, but genome-enabled approaches are rapidly advancing our understanding of this environmentally significant physiology.
1,219 citations
TL;DR: Microorganisms can enzymatically reduce a variety of metals in metabolic processes that are not related to metal assimilation, including technetium, vanadium, molybdenum, gold, silver, and copper, but reduction of these metals has not been studied extensively.
Abstract: Microorganisms can enzymatically reduce a variety of metals in metabolic processes that are not related to metal assimilation. Some microorganisms can conserve energy to support growth by coupling the oxidation of simple organic acids and alcohols, H2, or aromatic compounds to the reduction of Fe(III) or Mn(IV). This dissimilatory Fe(III) and Mn(IV) reduction influences the organic as well as the inorganic geochemistry of anaerobic aquatic sediments and ground water. Microorganisms that use U(VI) as a terminal electron acceptor play an important role in uranium geochemistry and may be a useful tool for removing uranium from contaminated environments. Se(VI) serves as a terminal electron acceptor to support anaerobic growth of some microorganisms. Reduction of Se(VI) to Se(O) is an important mechanism for the precipitation of selenium from contaminated waters. Enzymatic reduction of Cr(VI) to the less mobile and less toxic Cr(III), and reduction of soluble Hg(II) to volatile Hg(O) may affect the fate of these compounds in the environment and might be used as a remediation strategy. Microorganisms can also enzymatically reduce other metals such as technetium, vanadium, molybdenum, gold, silver, and copper, but reduction of these metals has not been studied extensively.
988 citations
References
More filters
TL;DR: Polycarbonate Nuclepore filters are better than cellulose filters for the direct counting of bacteria because they have uniform pore size and a flat surface that retains all of the bacteria on top of the filter.
Abstract: Polycarbonate Nuclepore filters are better than cellulose filters for the direct counting of bacteria because they have uniform pore size and a flat surface that retains all of the bacteria on top of the filter. Although cellulose filters also retain all of the bacteria, many are trapped inside the filter where they cannot be counted. Before use, the Nuclepore filters must be dyed with irgalan black to eliminate autofluorescence. Direct counts of bacteria in lake and ocean waters are twice as high with Nuclepore filters as with cellulose filters.
3,928 citations
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: In this paper, the chemistry of submerged soils is discussed and the role of lake, estuarine, and ocean sediments as reservoirs of nutrients for aquatic plants and as sinks for terrestrial wastes.
Abstract: Publisher Summary This chapter discusses the chemistry of submerged soils. The chemical changes in the submerged materials influence: (a) the character of the sediment or soil that forms, (b) the suitability of wet soils for crops, (c) the distribution of plant species around lakes and streams and in estuaries, deltas, and marine flood plains, (d) the quality and quantity of aquatic life, and (e) the capacity of lakes and seas to serve as sinks for terrestrial wastes. The single electrochemical property that serves to distinguish a submerged soil from a well-drained soil is its redox potential. The redox potential of a soil or sediment provides a quick, useful, semiquantitative measure of its oxidation–reduction status. Two recent developments have stimulated interest in the chemistry of submerged soils: the breeding of lowland rice varieties, with a high yield potential, and the pollution of streams, lakes, and seas, by domestic, agricultural, and industrial wastes. The chemistry of submerged soils is valuable: (a) in understanding the soil problems, limiting the performance of high-yielding rice varieties, and (b) in assessing the role of lake, estuarine, and ocean sediments as reservoirs of nutrients for aquatic plants and as sinks for terrestrial wastes.
2,651 citations
TL;DR: This is the first demonstration that microorganisms can completely oxidize organic compounds with Fe(III) or Mn(IV) as the sole electron acceptor and that oxidation of organic matter coupled to dissimilatory Fe( III), Mn( IV), or Mn (IV) reduction can yield energy for microbial growth.
Abstract: A dissimilatory Fe(III)- and Mn(IV)-reducing microorganism was isolated from freshwater sediments of the Potomac River, Maryland. The isolate, designated GS-15, grew in defined anaerobic medium with acetate as the sole electron donor and Fe(III), Mn(IV), or nitrate as the sole electron acceptor. GS-15 oxidized acetate to carbon dioxide with the concomitant reduction of amorphic Fe(III) oxide to magnetite (Fe(3)O(4)). When Fe(III) citrate replaced amorphic Fe(III) oxide as the electron acceptor, GS-15 grew faster and reduced all of the added Fe(III) to Fe(II). GS-15 reduced a natural amorphic Fe(III) oxide but did not significantly reduce highly crystalline Fe(III) forms. Fe(III) was reduced optimally at pH 6.7 to 7 and at 30 to 35 degrees C. Ethanol, butyrate, and propionate could also serve as electron donors for Fe(III) reduction. A variety of other organic compounds and hydrogen could not. MnO(2) was completely reduced to Mn(II), which precipitated as rhodochrosite (MnCO(3)). Nitrate was reduced to ammonia. Oxygen could not serve as an electron acceptor, and it inhibited growth with the other electron acceptors. This is the first demonstration that microorganisms can completely oxidize organic compounds with Fe(III) or Mn(IV) as the sole electron acceptor and that oxidation of organic matter coupled to dissimilatory Fe(III) or Mn(IV) reduction can yield energy for microbial growth. GS-15 provides a model for how enzymatically catalyzed reactions can be quantitatively significant mechanisms for the reduction of iron and manganese in anaerobic environments.
2,233 citations
TL;DR: Results indicate that iron reduction can outcompete methanogenic food chains for sediment organic matter when amorphous ferric oxyhydroxides are available in anaerobic sediments, and the transfer of electrons from organic matter to ferric iron can be a major pathway for organic matter decomposition.
Abstract: The potential for ferric iron reduction with fermentable substrates, fermentation products, and complex organic matter as electron donors was investigated with sediments from freshwater and brackish water sites in the Potomac River Estuary. In enrichments with glucose and hematite, iron reduction was a minor pathway for electron flow, and fermentation products accumulated. The substitution of amorphous ferric oxyhydroxide for hematite in glucose enrichments increased iron reduction 50-fold because the fermentation products could also be metabolized with concomitant iron reduction. Acetate, hydrogen, propionate, butyrate, ethanol, methanol, and trimethylamine stimulated the reduction of amorphous ferric oxyhydroxide in enrichments inoculated with sediments but not in uninoculated or heat-killed controls. The addition of ferric iron inhibited methane production in sediments. The degree of inhibition of methane production by various forms of ferric iron was related to the effectiveness of these ferric compounds as electron acceptors for the metabolism of acetate. The addition of acetate or hydrogen relieved the inhibition of methane production by ferric iron. The decrease of electron equivalents proceeding to methane in sediments supplemented with amorphous ferric oxyhydroxides was compensated for by a corresponding increase of electron equivalents in ferrous iron. These results indicate that iron reduction can outcompete methanogenic food chains for sediment organic matter. Thus, when amorphous ferric oxyhydroxides are available in anaerobic sediments, the transfer of electrons from organic matter to ferric iron can be a major pathway for organic matter decomposition.
1,360 citations