Chemolithotrophic and Autotrophic Growth of Thermothrix thiopara and Some Thiobacilli on Thiosulphate and Polythionates, and a Reassessment of the Growth Yields of Thx. thiopara in Chemostat Culture

Mason, Jonathan; Kelly, Donovan P.; Wood, Ann P.

doi:10.1099/00221287-133-5-1249

Cited by 16 publications

(12 citation statements)

References 19 publications

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“…Its growth on the one-carbon organosulfur compounds carbon disulfide and carbonyl sulfide must also be autotrophic, but the biochemistry of its growth on dimethyl sulfide and methanethiol has not been investigated. Its growth yields on autotrophic substrates are comparable to those seen with Paracoccus versutus (Kelly et al 1979;Kelly andWood 1982, 1984;Kraczkiewicz-Dowjat and Kelly 1991) and Paracoccus denitrificans (Jordan et al 1995;Jordan 1996;Kelly and Wood 1996), but our results are the first to show that the autotrophic yield on thiosulfate as the sole energy substrate is of the same order as those for some Paracoccus and Thiobacillus species Mason et al 1987;Kelly 1990). The 10-to 20-fold stimulation by bicarbonate of the poor growth yields on the one-carbon methylotrophic substrates methylamine and methanol was indicative of the absence of a carbon-dioxide-concentrating mechanism from this organism, as seen with autotrophic P. versutus (Karagouni and Kelly 1989), and also indicates the importance of carbon dioxide for growth on these substrates.…”

Section: Discussionsupporting

confidence: 87%

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Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis

Kelly

1998

Archives of Microbiology

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Xanthobacter tagetidis grew as a chemolithotrophic autotroph on thiosulfate and other inorganic sulfur compounds, as a heterotroph on thiophene-2-carboxylic acid, acetic acid and alpha-ketoglutaric acid, and as a mixotroph on thiosulfate in combination with thiophene-2-carboxylic acid and/or acetic acid. Autotrophic growth on one-carbon organosulfur compounds, and intermediates in their oxidation are also reported. Thiosulfate enhanced the growth yields in mixotrophic cultures, presumably by acting as a supplementary energy source, since ribulose bisphosphate carboxylase was only active in thiosulfate-grown cells and was not detected in mixotrophic cultures using thiosulfate with thiophene-2-carboxylic acid. Bacteria grown on thiophene-2-carboxylic acid also oxidized sulfide, thiosulfate and tetrathionate, indicating these as possible sulfur intermediates in thiophene-2-carboxylic acid degradation. Thiosulfate and tetrathionate were oxidized completely to sulfate and, consequently, did not accumulate as products of thiophene-2-carboxylic acid oxidation in growing cultures. Km and Vmax values for the oxidation of thiosulfate, tetrathionate or sulfide were 13 &mgr;M and 83 nmol O2 min-1 (mg dry wt.)-1, respectively; thiosulfate and tetrathionate became autoinhibitory at concentrations above 100 &mgr;M. The true growth yield (Ymax) on thiophene-2-carboxylic acid was estimated from chemostat cultures (at dilution rates of 0.034-0.094 h-1) to be 112.2 g mol-1, with a maintenance coefficient (m) of 0.3 mmol thiophene-2-carboxylic acid (g dry wt.)-1 h-1, and the maximum specific growth rate (&mgr;max) was 0.116 h-1. Growth in chemostat culture at a dilution rate of 0. 041 h-1 indicated growth yields [g dry wt. (mol substrate)-1] of 8.1 g (mol thiosulfate)-1, 60.9 g (mol thiophene-2-carboxylic acid)-1, and 17.5 g (mol acetic acid)-1, with additive yields for growth on mixtures of these substrates. At a dilution rate of 0.034 h-1, yields of 57.8 g (mol alpha-ketoglutaric acid)-1 and 60.7 g (mol thiophene-2-carboxylic acid)-1 indicated some additional energy conservation from oxidation of the thiophene-sulfur. SDS-PAGE of cell-free preparations indicated a polypeptide (Mr, 21.0 kDa) specific to growth on thiophene-2-carboxylic acid for which no function can yet be ascribed: no metabolism of thiophene-2-carboxylic acid by cell-free extracts was detected. It was shown that X. tagetidis exhibits a remarkable degree of metabolic versatility and is representative of facultatively methylotrophic and chemolithotrophic autotrophs that contribute significantly to the turnover of simple inorganic and organic sulfur compounds (including substituted thiophenes) in the natural environment.

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Section: Discussionsupporting

confidence: 87%

“…-1 ] against dilution rate (Fieschko and Humphrey 1984;Mason et al 1987). To determine the growth yield on hydrogen in the presence of a growth-limiting quantity of oxygen, batch cultures (25 ml in sealed 300-ml flasks) were provided with bicarbonate (10 mM) and a gas mixture of 10 parts oxygen and 90 parts hydrogen.…”

Section: Methodsmentioning

confidence: 99%

Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis

Kelly

1998

Archives of Microbiology

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“…This is comparable to growth yields observed for other (facultative) autotrophic sulfide/ thiosulfate oxidizing Proteobacteria that range from 2.5 to 16 g DW mol -1 (data not corrected for dissimilated substrate) (Table S1). Also, the sulfide and thiosulfate respiration rates, maximum growth rates and maintenance coefficients are in the range observed for this type of organisms (Mason et al, 1987;Sorokin et al, 2003;Banciu et al, 2004). Table S1 lists growth yields and maximum growth rates for neutrophilic, mesophilic sulfuroxidizing Proteobacteria.…”

Section: Characterization Of Autotrophic Growthmentioning

confidence: 84%

Reduced inorganic sulfur oxidation supports autotrophic and mixotrophic growth of Magnetospirillum strain J10 and Magnetospirillum gryphiswaldense

Geelhoed

Kleerebezem

Sorokin

et al. 2010

Environmental Microbiology

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Magnetotactic bacteria are present at the oxic-anoxic transition zone where opposing gradients of oxygen and reduced sulfur and iron exist. Growth of non-magnetotactic lithoautotrophic Magnetospirillum strain J10 and its close relative magnetotactic Magnetospirillum gryphiswaldense was characterized in microaerobic continuous culture. Both strains were able to grow in mixotrophic (acetate + sulfide) and autotrophic (sulfide or thiosulfate) conditions. Autotrophically growing cells completely converted sulfide or thiosulfate to sulfate and produced 7.5 g dry weight per mol substrate at a maximum observed growth rate of 0.09 h(-1) for strain J10 and 0.07 h(-1) for M. gryphiswaldense. The respiratory activity for acetate was repressed in autotrophic and also in mixotrophic cultures, suggesting acetate was used as C-source in the latter. We have estimated the proportions of substrate used for assimilatory processes and evaluated the biomass yields per mol dissimilated substrate. The yield for lithoheterotrophic growth using acetate as the C-source was approximately twice the autotrophic growth yield and very similar to the heterotrophic yield, showing the importance of reduced sulfur compounds for growth. In the draft genome sequence of M. gryphiswaldense homologues of genes encoding a partial sulfur-oxidizing (Sox) enzyme system and reverse dissimilatory sulfite reductase (Dsr) were identified, which may be involved in the oxidation of sulfide and thiosulfate. Magnetospirillum gryphiswaldense is the first freshwater magnetotactic species for which autotrophic growth is shown.

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“…The facultative autotroph T. acidophilus is capable of heterotrophic growth on glucose and various other simple organic compounds (7,22). Autotrophic growth can be supported by a variety of inorganic sulfur compounds (7,15,20) and formate (J. T. Pronk, P. de Bruijn, J. P. van Dijken, P. Bos, and J. G. Kuenen, Arch. Microbiol., in press).…”

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confidence: 99%

Mixotrophic and Autotrophic Growth of Thiobacillus acidophilus on Glucose and Thiosulfate

Pronk

Meulenberg

Berg

et al. 1990

Appl Environ Microbiol

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Mixotrophic growth of the facultatively autotrophic acidophile Thiobacillus acidophilus on mixtures of glucose and thiosulfate or tetrathionate was studied in substrate-limited chemostat cultures. Growth yields in mixotrophic cultures were higher than the sum of the heterotrophic and autotrophic growth yields. Pulse experiments with thiosulfate indicated that tetrathionate is an intermediate during thiosulfate oxidation by cell suspensions of T. acidophilus. From mixotrophic growth studies, the energetic value of thiosulfate and tetrathionate redox equivalents was estimated to be 50% of that of redox equivalents derived from glucose oxidation. Ribulose 1,5-bisphosphate carboxylase (RuBPCase) activities in cell extracts and rates of sulfur compound oxidation by cell suspensions increased with increasing thiosulfate/glucose ratios in the influent medium of the mixotrophic cultures. Significant RuBPCase and sulfur compound-oxidizing activities were detected in heterotrophically grown T. acidophilus. Polyhedral inclusion bodies (carboxysomes) could be observed at low frequencies in thin sections of cells grown in heterotrophic, glucose-limited chemostat cultures. Highest RuBPCase activities and carboxysome abundancy were observed in cells from autotrophic, C02limited chemostat cultures. The maximum growth rate at which thiosulfate was still completely oxidized was increased when glucose was utilized simultaneously. This, together with the fact that even during heterotrophic growth the organism exhibited significant activities of enzymes involved in autotrophic metabolism, indicates that T. acidophilus is well adapted to a mixotrophic lifestyle. In this respect, T. acidophilus may have a competitive advantage over autotrophic acidophiles with respect to the sulfur compound oxidation in environments in which organic compounds are present.

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Chemolithotrophic and Autotrophic Growth of Thermothrix thiopara and Some Thiobacilli on Thiosulphate and Polythionates, and a Reassessment of the Growth Yields of Thx. thiopara in Chemostat Culture

Cited by 16 publications

References 19 publications

Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis

Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis

Reduced inorganic sulfur oxidation supports autotrophic and mixotrophic growth of Magnetospirillum strain J10 and Magnetospirillum gryphiswaldense

Mixotrophic and Autotrophic Growth of Thiobacillus acidophilus on Glucose and Thiosulfate

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