Methylated Sulfur Compounds inMicrobial Mats:InSitu Concentrations andMetabolism byaColorless Sulfur Bacterium
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Abstract:
Theconcentrations ofthevolatile organic sulfur compounds methanethiol, dimethyl disulfide, anddimethyl sulfide (DMS)andtheviable population capable ofDMS utilization inlaminated microbial ecosystems were evaluated. Significant levels ofDMS anddimethyl disulfide (maximum concentrations of220and24nmolcm3 ofsediment-', respectively) couldbedetected onlyatthetop20mm ofthemicrobial mat,whereas methanethiol wasfoundonlyatdepth horizons from20to50mm (maximum concentration of42nmolcm3of sediment- l).DMS concentrations inthesurface layer doubled after coldhydrolysis ofitsprecursor, dimethylsulfoniopropionate. Most-probable-number counts revealed 2.2x 105cells cm3ofsediment-', inthe 0-to5-mm depthhorizon, capable ofgrowthon DMS asthesolesourceofenergy. An obligately chemolithoautotrophic bacillus designated strain T5wasisolated fromthetoplayer ofthemarine sediment. Continuous culture studies inwhichDMS wasthegrowth-limiting substrate revealed amaximumspecific growth rateof0.10h-1andasaturation constant of90,umol liter-' foraerobic growth onthis substrate. Microbial decomposition ofsulfur-containing aminoacidsKeywords:
Methanethiol
Dimethylsulfoniopropionate
Dimethyl sulfide
Limiting
Isotopes of sulfur
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Anaerobic enrichment cultures with H2S and N2O as substrates which were inoculated with a biofilm sample showed rapid growth and gas formation after 2 to 3 days at 27 degrees C. By using the deep-agar dilution technique, a pure culture was obtained. The strain was tentatively identified as Thiobacillus denitrificans. The isolate was used for batch and gradient culture studies under denitrifying conditions, oxidizing H2S with concomitant reduction of N2O to N2. In batch culture, oxidation of H2S was stepwise, with transient accumulation of elemental sulfur; the final oxidation product was SO4(2-). In gradient culture, there was no notable accumulation of elemental sulfur and microsensor measurements of H2S and N2O showed that H2S was oxidized directly to SO4(2-). In the presence of C2H2, however, oxidation of H2S stopped at the level of elemental sulfur and no SO4(2-) was produced in either batch or gradient cultures. This is a hitherto unknown inhibitory effect of C2H2. The inhibition is suggested to occur at the level of sulfite reductase, which catalyzes the oxidation of elemental sulfur to SO3(2-) in T. denitrificans. However, reduction of N2O in this strain was, surprisingly, not affected by C2H2. The isolate is the first chemolithoautotrophic organism shown to reduce N2O in the presence of C2H2. Denitrification in natural ecosystems is often quantified as N2O accumulation after C2H2 addition. However, the presence of large numbers of similar organisms with C2H2-insensitive N2O reduction could lead to underestimation of in situ rates.
Thiobacillus
Enrichment culture
Paracoccus denitrificans
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The colorless sulfur bacterium Thiobacillus thioparus T5, isolated from a marine microbial mat, was grown in continuous culture under conditions ranging from sulfide limitation to oxygen limitation. Under sulfide-limiting conditions, sulfide was virtually completely oxidized to sulfate. Under oxygen-limiting conditions, sulfide was partially oxidized to zerovalent sulfur (75%) and thiosulfate (17%). In addition, low concentrations of tetrathionate and polysulfide were detected. The finding of in vivo thiosulfate formation supports the discredited observations of thiosulfate formation in cell free extracts in the early sixties. In a microbial mat most sulfide oxidation was shown to take place under oxygen-limiting conditions. It is suggested that zerovalent sulfur formation by thiobacilli is a major process resulting in polysulfide accumulation. Implications for the competition between colorless sulfur bacteria and purple sulfur bacteria are discussed.
Thiobacillus
Tetrathionate
Polysulfide
Sulfur Cycle
Sodium thiosulfate
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Thiobacillus
Autotroph
Thiobacillus ferrooxidans
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Removal of organic and inorganic sulfur compounds from sour gases is required because of their toxicity and atmospheric pollution. The most common are hydrogen sulfide (H2S) and methanethiol (MT). Under oxygen-limiting conditions about 92 mol% of sulfide is oxidized to sulfur by haloalkaliphilic sulfur-oxidizing bacteria (SOB), whilst the remainder is oxidized either biologically to sulfate or chemically to thiosulfate. MT is spontaneously oxidized to dimethyl disulfide (DMDS), which was found to inhibit the oxidation of sulfide to sulfate. Hence, we assessed the effect of DMDS on product formation in a lab-scale biodesulfurization setup. DMDS was quantified using a newly, in-house developed analytical method. Subsequently, a chemical reaction mechanism was proposed for the formation of methanethiol and dimethyl trisulfide from the reaction between sulfide and DMDS. Addition of DMDS resulted in significant inhibition of sulfate formation, leading to 96 mol% of sulfur formation. In addition, a reduction in the dominating haloalkaliphilic SOB species, Thioalkalivibrio sulfidiphilus, was observed in favor of Thioalkaibacter halophilus as a more DMDS-tolerant with the 50 % inhibition coefficient at 2.37 mM DMDS.
Methanethiol
Dimethyl sulfide
Dimethyl trisulfide
Sour gas
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The effects of Thiobacillus denitrificans combined with signal molecules on the removal of sulfide and nitrate was investigated. By adding signal molecules and T. denitrificans at the same, the total number of microorganisms increased, the removal of sulfide and nitrate was accelerated, and an increase in nitrogen gas and more stable accumulation of elemental sulfur was observed. The total number of microorganisms after the reaction was detected using fluorescence in situ hybridization (FISH) technique. In this experiment, the optimal concentration for the stable accumulation of elemental sulfur from six concentrations of signal molecules was revealed. Further, the effects of adding signal molecules, T. denitrificans, and their combination were analyzed at this concentration. The results showed that it was easier to accumulate elemental sulfur after the addition of 1.0 μmol·L-1 signal molecule. After adding both T. denitrificans and 1.0 μmol·L-1 signal molecules at a sulfide concentration of 200 mg·L-1, the removal of sulfide and nitrate increased to 99.8% and 96.9% at 72 h, respectively, and increases in nitrogen gas and sulfur were observed. The amounts of elemental sulfur and nitrogen gas reached to 59.0 mg and 80.0 mL, respectively, after adding 2.5 μmol·L-1 signal molecules at 72 h when the sulfide concentration was 300 mg·L-1. Under those conditions, the removal efficiency of sulfide and nitrate reached 99.0% and 93.9%, and the production of elemental sulfur and nitrogen reached 63.1 mg and 79.5 mL, respectively.
Thiobacillus
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The concentrations of the volatile organic sulfur compounds methanethiol, dimethyl disulfide, and dimethyl sulfide (DMS) and the viable population capable of DMS utilization in laminated microbial ecosystems were evaluated. Significant levels of DMS and dimethyl disulfide (maximum concentrations of 220 and 24 nmol cm3 of sediment-1, respectively) could be detected only at the top 20 mm of the microbial mat, whereas methanethiol was found only at depth horizons from 20 to 50 mm (maximum concentration of 42 nmol cm3 of sediment-1). DMS concentrations in the surface layer doubled after cold hydrolysis of its precursor, dimethylsulfoniopropionate. Most-probable-number counts revealed 2.2 x 10(5) cells cm3 of sediment-1, in the 0- to 5-mm depth horizon, capable of growth on DMS as the sole source of energy. An obligately chemolithoautotrophic bacillus designated strain T5 was isolated from the top layer of the marine sediment. Continuous culture studies in which DMS was the growth-limiting substrate revealed a maximum specific growth rate of 0.10 h-1 and a saturation constant of 90 mumol liter-1 for aerobic growth on this substrate.
Methanethiol
Dimethylsulfoniopropionate
Dimethyl sulfide
Bacterial growth
Saturation (graph theory)
Microbial mat
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Intact cells of Thiobacillus ferrooxidans NASF-1 incubated under anaerobic conditions in a reaction mixture containing 0.5% colloidal sulfur produced hydrogen sulfide (H2S) extracellularly. The amount of H2S produced by cells increased corresponding to the cell amounts and colloidal sulfur. Two activity peaks of H2S production were observed at pH 1.5 and 7.5. We tentatively called the enzyme activities pH 1.5- and pH 7.5-sulfur reducing systems, respectively. Seven strains of T. ferrooxidans tested had both the activities of pH 1.5- and pH 7.5-sulfur reducing systems, but at different levels. T. ferrooxidans NASF-1 showed the highest activity of the pH 1.5-sulfur reducing system and strain 13598 from ATCC showed the highest activity of the pH 7.5-sulfur reducing system. Further characteristics of H2S production were studied with intact cells of NASF-1. The optimum temperatures for pH 1.5- and pH 7.5-sulfur reducing systems of NASF-1 were 40°C. Hydrogen sulfide production continued for 8 days and total amounts of H2S produced at pH 7.5 and 1.5 were 832 and 620 nmol/mg protein, respectively. The pH 7.5-sulfur reducing system used only colloidal sulfur as the electron acceptor. However, the pH 1.5-sulfur reducing system used both colloidal sulfur and tetrathionate. Thiosulfate, dithionate, and sulfite could not be used as the electron acceptor for both of the sulfur reducing systems. Potassium cyanide activated by 3- fold the pH 1.5-sulfur reducing system activity at 0.5 mM but did not affect the activity of the pH 7.5-sulfur reducing system. An inhibitor of sulfite reductase, p-chloromercuribenzene sulfonic acid, did not affect either enzyme activity. Sodium molybdate and monoiodoacetic acid strongly inhibited the activity of the pH 1.5-sulfur reducing system at 1.0 mM, but not the activity of pH 7.5-sulfur reducing system.
Tetrathionate
Electron acceptor
Reducing agent
Thiobacillus
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Sulfur-reducing bacteria are promising agents for the development of new methods of wastewater treatment with the removal of ions of heavy metals and organic compounds. Study of the effect of various environmental factors on the growth and sulfidogenic activity of sulfur-reducing bacteria allows one to investigate the adaptability of these microorganisms to stress factors. The paper deals with the effect of рН, different concentrations of elemental sulfur, hydrogen sulfide and presence of various electron acceptors on the growth and sulfidogenic activity of bacteria Desulfuromonas sp. YSDS-3. The calculation of C/S ratio for sulfur-reducing bacteria Desulfuromonas sp. YSDS-3 was made, with the comparison with similar parameters of sulfate-reducing bacteria. In the medium with elemental sulfur, concentration of hydrogen sulfide increased with the concentration of elemental sulfur. Bacteria Desulfuromonas sp. YSDS-3 accumulated their biomass in the most effective way at the concentration of elemental sulfur of 10–100 mM. In the medium with polysulfide form of sulfur at the neutral pH, bacteria produced hydrogen sulfide and accumulated biomass the best. Hydrogen sulfide at the concentration of 3 mM did not inhibit the bacterial growth, but further increase in the hydrogen sulfide concentration inhibited the growth of bacteria. The bacteria did not grow at the hydrogen sulfide concentration of 25 mM and above. As the concentration of elemental sulfur and cell density increases, sulfidogenic activity of the bacteria grows. Presence of two electron acceptors (S and K2Cr2O7, S and MnO2, S and Fe (III)) did not affect the accumulation of biomass of the bacteria Desulfuromonas sp. YSDS-3. However, under such conditions the bacteria accumulated 1.5–2.5 times less hydrogen sulfide than in the test medium. After 12–24 h of cultivation, different concentrations of elemental sulfur had a significant effect on the sulfidogenic activity. However, during 3–16 days of cultivation, the percentage of effect of elemental sulfur concentration decreased to 31%, while the percentage of effect of cell density increased threefold. Presence in the medium of the electron acceptors (Cr (VI), MnO2, Fe (III)) alternative to elemental sulfur led to a significant decrease in the content of hydrogen sulfide produced by sulfur-reducing bacteria.
Sulfate-Reducing Bacteria
Acidithiobacillus thiooxidans
Polysulfide
Electron acceptor
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Several low-molecular-weight sulfonates were added to microbial mat slurries to investigate their effects on sulfate reduction. Instantaneous production of sulfide occurred after taurine and cysteate were added to all of the microbial mats tested. The rates of production in the presence of taurine and cysteate were 35 and 24 microM HS(-) h(-1) in a stromatolite mat, 38 and 36 microM HS(-) h(-1) in a salt pond mat, and 27 and 18 microM HS(-) h(-1) in a salt marsh mat, respectively. The traditionally used substrates lactate and acetate stimulated the rate of sulfide production 3 to 10 times more than taurine and cysteate stimulated the rate of sulfide production in all mats, but when ethanol, glycolate, and glutamate were added to stromatolite mat slurries, the resulting increases were similar to the increases observed with taurine and cysteate. Isethionate, sulfosuccinate, and sulfobenzoate were tested only with the stromatolite mat slurry, and these compounds had much smaller effects on sulfide production. Addition of molybdate resulted in a greater inhibitory effect on acetate and lactate utilization than on sulfonate use, suggesting that different metabolic pathways were involved. In all of the mats tested taurine and cysteate were present in the pore water at nanomolar to micromolar concentrations. An enrichment culture from the stromatolite mat was obtained on cysteate in a medium lacking sulfate and incubated anaerobically. The rate of cysteate consumption by this enrichment culture was 1.6 pmol cell(-1) h(-1). Compared to the results of slurry studies, this rate suggests that organisms with properties similar to the properties of this enrichment culture are a major constituent of the sulfidogenic population. In addition, taurine was consumed at some of highest dilutions obtained from most-probable-number enrichment cultures obtained from stromatolite samples. Based on our comparison of the sulfide production rates found in various mats, low-molecular-weight sulfonates are important sources of C and S in these ecosystems.
Sodium lactate
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Enrichment cultures of phototrophic purple bacteria rapidly oxidized up to 10 mM dimethyl sulfide (DMS) to dimethyl sulfoxide (DMSO). DMSO was qualitatively identified by proton nuclear magnetic resonance. By using a biological assay, DMSO was always quantitatively recovered from the culture media. DMS oxidation was not detected in cultures incubated in the dark, and it was slow in cultures exposed to full daylight. Under optimal conditions, the second-order rate constant for DMS oxidation was 6 day −1 mg of protein −1 ml −1 . The rate constant was reduced in the presence of high concentration of sulfide (>1 mM), but was not affected by the addition of acetate. DMS was also oxidized to DMSO by a pure strain (tentatively identified as a Thiocystis sp.) isolated from the enrichment cultures. DMS supported growth of the enrichment cultures and of the pure strain by serving as an electron source for photosynthesis. A determination of the amount of protein produced in the cultures and an estimation of the electron balance suggested that the two electrons liberated during the oxidation of DMS to DMSO were quantitatively used to reduce carbon dioxide to biomass. The oxidation of DMS by phototrophic purple bacteria may be an important source of DMSO detected in anaerobic ponds and marshes.
Dimethyl sulfide
Electron donor
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Citations (105)