Summary
Suspensions ofThiobacillus ferrooxidans in Warburg flasks oxidized ferrous iron and coupled14CO2 fixation to the oxidation. The sulphates of zinc, cobalt, copper, nickel or uranium (0.1–1.0 M) depressed the rate of Fe2+ oxidation: nickel and uranyl ions were the most inhibitory. Uranyl, copper and nickel ions inhibited iron-dependent CO2-fixation, the two former producing a marked uncoupling effect on CO2-fixation, similar to that produced by 2:4-dinitrophenol. Molybdate also inhibited iron oxidation. Incorporation of14C-labelled amino acids and glucose was largely dependent on energy from ferrous-iron oxidation and was also strongly inhibited by uranyl sulphate. Kinetic analysis of the inhibition of iron-oxidation by uranium indicated mixed competitive and non-competitive inhibition. Little binding of238U,63Ni or59Fe toT. ferrooxidans was observed and the effects of uranium were concluded to result mainly from loose binding at sites on the cell membrane concerned with iron-oxidation and possibly the transport of other metals. Molybdate probably interfered with sulphate-dependent steps of iron oxidation. Uncoupling of CO2-fixation probably resulted in part from interference with energy metabolism and could depend on transport of uranyl ions through the cell membrane. CO2-fixation by an uraniumtolerant culture (U+) was less sensitive to uranyl-inhibition than that by the wild-type strain (U−), but iron oxidation and CO2-fixation were much more sensitive to uranium when the U− organisms were previously cultured on thiosulphate rather than ferrous iron.
Similar content being viewed by others
References
Abelson, P. H., Aldous, E.: Ion antagonisms in microorganisms: interference of normal magnesium metabolism by nickel, cobalt, cadmium, zinc and manganese. J. Bact.60, 401–413 (1950)
Aleem, M. I. H.: Generation of reducing power in chemosynthesis. IV. Energylinked reduction of pyridine nucleotides by succinate inThiobacillus novellus. Biochim. Biophys. Acta128, 1–12 (1966)
Archibald, A. R., Baddiley, J., Heptinstall, S.: The alanine ester content and magnesium binding capacity of walls ofStaphylococcus aureus H grown at different pH values. Biochim. biophys. Acta (Amst.)291, 629–634 (1973)
Armstrong, W. McD., Rothstein, A.: Discrimination between alkali metal cations by yeast. J. gen. Physiol.48, 61–71 (1964)
Beck, J. V., Shafia, F. M.: Effect of phosphate-ion and 2,4-dinitrophenol on the activity of intact cells ofThiobacillus ferrooxidans. J. Bact.88, 850–857 (1964)
Bhappu, R. B., Reynolds, D. H., Roman, R. J.: Molybdenum recovery from sulfide and oxide ores. J. Metals17, 1199–1205 (1965)
Bounds, H. C., Colmer, A. R.: Comparison of the kinetics of thiosulfate oxidation by three iron-sulfur oxidizers. Canad. J. Microbiol.18, 735–740 (1972)
Brierley, C. L., Murr, L. E.: Leaching: use of a thermophilic and chemoautotrophic microbe. Science179, 488–490 (1973)
Chopra, I.: Decreased uptake of cadmium by a resistant strain ofStaphylococcus aureus. J. gen. Microbiol.63, 265–267 (1971)
Cobet, A. B., Jones, G. E., Albright, J., Simon, H., Wirsen, C.: The effect of nickel on a marine bacterium: fine structure ofArthrobacter marinus. J. gen. Microbiol.66, 185–196 (1971)
Dugan, P. R., Lundgren, D. G.: Energy supply for the chemoautotrophFerrobacillus ferrooxidans. J. Bact.89, 825–834 (1965)
Duncan, D. W., Bruynesteyn, A.: Microbiological leaching of uranium. New Mexico Bur. Mines Miner. Res., Circ.118, 55–61 (1971)
Fuhrmann, G. F., Rothstein, A.: The transport of Zn2+, Co2+ and Ni2+ into yeast cells. Biochim. biophys. Acta (Amst.)163, 325–330 (1968)
Kamalov, M. R.: Adaptation ofThiobacillus ferrooxidans culture to increased amounts of copper, zinc and molybdenum in acid medium. Izv. Akad. Nauk Kaz. SSR, Ser. Biol.10, 39–44 (1972)
Kelly, D. P.: The incorporation of acetate by the chemoautotrophThiobacillus neapolitanus strain C. Arch. Mikrobiol.58, 99–116 (1967)
Kelly, D. P.: Biochemistry of oxidation of inorganic sulphur compounds by microorganisms. Austr. J. Sci.31, 165–173 (1968)
Kelly, D. P., Syrett, P. J.: The effect of uncoupling agents on carbon dioxide fixation by aThiobacillus. J. gen. Microbiol.34, 307–317 (1964)
Kelly, D. P., Syrett, P. J.: Energy coupling during sulphur compound oxidation byThiobacillus sp. strain C. J. gen. Microbiol.43, 109–118 (1966)
Kotyk, A., Michaljaničova, D., Saiyid, N. H.: Effect of uranyl ions on steady state distribution of monosaccharides in Baker's yeast. Folia microbiol. (Praha)16, 355–358 (1971a)
Kotyk, A., Říhová, L., Ponec, M.: Uptake of amino acids by actidione-treated yeast cells. II. Effect of incubation conditions and metabolic inhibitors. Folia microbiol. (Praha)16, 445–450 (1971b)
Lazaroff, N.: Sulfate requirement for iron oxidation byThiobacillus ferrooxidans. J. Bact.85, 78–83 (1963)
Lusk, J. E., Kennedy, E. P.: Magnesium transport inEscherichia coli. J. biol. Chem.244, 1653–1655 (1973)
Lusk, J. E., Nelson, D. L.: Effects of colicins E1 and K on permeability to magnesium and cobaltous ions. J. Bact.112, 148–160 (1972)
Maxwell, W. A., Metzler, R., Spoerl, E.: Uranyl nitrate inhibition of transport systems inSaccharomyces cerevisiae. J. Bact.105, 1205–1206 (1971)
Paton, W. H. N., Budd, K.: Zinc uptake inNeocosmospora vasinfecta. J. gen. Microbiol.72, 173–184 (1972)
Peck, H. D.: Symposium on metabolism of inorganic compounds. V. Comparative metabolism of inorganic sulfur compounds in microorganisms. Bact. Rev.26, 67–94 (1962)
Roberts, R. B., Abelson, P. H., Cowie, D. B., Bolton, E. J., Britten, R. J.: Studies of biosynthesis inEscherichia coli. Washington D.C.: Carnegie Institution of Washington Publication 1955
Rothstein, A.: Enzyme system of the cell surface involved in the uptake of sugars by yeast. Symp. Soc. exp. Biol.8, 165–201 (1954)
Rothstein, A., Meier, R.: The relationship of the cell surface to metabolism. VI. The chemical nature of uranium-complexing groups of the cell surface. J. cell. comp. Physiol.38, 245–270 (1951)
Roy, A., Trudinger, P. A.: The biochemistry of inorganic compounds of sulphur. Cambridge: University Press 1970
Sadler, W. R., Trudinger, P. A.: The inhibition of microorganisms by heavy metals. Miner. Depos.2, 158–168 (1967)
Saiyid, N. H., Kotyk, A.: Amino acid transport inRhodotorula utilis. Folia microbiol. (Praha)17, 261–268 (1972)
Saxena, J., Aleem, M. I. H.: Generation of reducing power in chemosynthesis. VII. Mechanism of pyridine nucleotide reduction by thiosulfate in the chemoauthotrophThiobacillus neapolitanus. Arch. Mikrobiol.84, 317–326 (1972)
Schnaitman, C. A., Korczynski, M. S., Lundgren, D. G.: Kinetic studies of iron oxidation by whole cells ofFerrobacillus ferrooxidans. J. Bact.99, 552–557 (1969)
Silver, M., Johnseine, P., Whitney, E., Clark, D.: Manganese-resistant mutants ofEscherichia coli: physiological and genetic studies. J. Bact.110, 186–195 (1972)
Tuovinen, O. H.: Microbiological aspects in the leaching of uranium byThiobacillus ferrooxidans. Atomic Energy Rev.10, 251–258 (1972)
Tuovinen, O. H., Kelly, D. P.: Biology ofThiobacillus ferrooxidans in relation to the microbiological leaching of sulphide ores. Z. allg. Mikrobiol.12, 311–346 (1972)
Tuovinen, O. H., Kelly, D. P.: Studies on the growth ofThiobacillus ferrooxidans. I. Use of membrane filters and ferrous iron agar to determine viable numbers, and comparison with14CO2-fixation and iron oxidation as measures of growth. Arch. Mikrobiol.88, 285–298 (1973)
Tuovinen, O. H., Kelly, D. P.: Studies on the growth ofThiobacillus ferrooxidans. II. Toxicity of uranium to growing cultures and tolerance conferred by mutation, other metal ions and EDTA. Arch. Microbiol.95, 153–164 (1974)
Tuovinen, O. H., Niemelä, S. I., Gyllenberg, H. G.: Tolerance ofThiobacillus ferrooxidans to some metals. Antonie v. Leeuwenhoek37, 489–496 (1971a)
Tuovinen, O. H., Niemelä, S. I., Gyllenberg, H. G.: Effect of mineral nutrients and organic substances on the development ofThiobacillus ferrooxidans. Biotechnol. Bioeng.13, 517–527 (1971b)
Umbreit, W. W., Burris, R. H., Stauffer, N.: Manometric techniques, 4th ed. Minneapolis, Minn.: Burgess 1964
van Steveninck, J., Booij, H. L.: The role of polyphosphates in the transport mechanism of glucose in yeast cells. J. gen. Physiol.48, 43–60 (1964)
Webb, M.: The mechanism of acquired resistance to Co2+ and Ni2+ in grampositive and gram-negative bacteria. Biochim. biophys. Acta (Amst.)222, 440–446 (1970)
Willecke, K., Gries, E.-M., Oehr, P.: Coupled transport of citrate and magnesium inBacillus subtilis. J. biol. Chem.248, 807–814 (1973)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Tuovinen, O.H., Kelly, D.P. Studies on the growth ofThiobacillus ferrooxidans . Arch. Microbiol. 95, 165–180 (1974). https://doi.org/10.1007/BF02451758
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF02451758