Abstract
The results of ecophysiological studies on obligately and facultatively chemolithotrophic thiobacilli performed over the past years clearly show that the two types of organisms occupy different ecological niches. Chemostat experiments with cultures of the obligate chemolithotroph Thiobacillus neapolitanus and the facultative chemolithotroph Thiobacillus A2 have been carried out to explain the competitiveness of T. neapolitanus under conditions of strongly fluctuating substrate supply.
Thiobacillus neapolitanus appeared to be very resistant to starvation periods whereafter it could oxidize sulfide (or thiosulfate) almost instantaneously at the original rate. Under alternate supply of 4 h sulfide and 4 h sulfate (or acetate which does not support growth of the organism either) to a chemostat culture of T. neapolitanus (D=0.05 h−1) the sulfide concentration in the growth vessel never reached levels higher than 4μm. This strategy is aimed at maximal reactivity. In contrast to T. neapolitanus the facultative chemolithotroph T.A2 appeared to be very flexible with respect to its energy generation. Under alternate supply of 4 h sulfide and 4 h acetate (D=0.05 h−1) T.A2 was able to grow continuously since it directed its metabolism to either heterotrophy or autotrophy by rapid induction-repression mechanisms. This flexible strategy seems to be incompatible with a reactive strategy within one organism, since the oxidation capacity for sulfide decreased during the acetate period resulting in accumulation of sulfide during the sulfide period. It is concluded that T.A2 needs a continuous supply of an inorganic and an organic substrate to thrive whereas T. neapolitanus needs only a continuous supply of a reduced inorganic sulfur source but also will persist in environments with interrupted addition of sulfide provided that the starvation period does not last too long.
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References
Beudeker, R. F. Cannon, G. C., Kuenen, J. G. and Shively, J. M. 1980. Relations between D-ribulose-1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. — Arch. Microbiol. 124: 185–189.
Beudeker, R. F., Codd, G. A. and Kuenen, J. G. 1981a. Quantification and intracellular distribution of ribulose-1,5-bisphosphate carboxylase in Thiobacillus neapolitanus, as related to possible functions of carboxysomes. — Arch. Microbiol. 129: 361–367.
Beudeker, R. F., Kerver, J. W. M. and Kuenen, J. G. 1981b. Occurrence, structure and function of intracellular polyglucose in the obligately chemolithotroph Thiobacillus neapolitanus. —Arch. Microbiol. 129: 221–226.
Beudeker, R. F., Kuenen, J. G. and Codd, G. A. 1981c. Glycollate metabolism in the obligate chemolithotroph Thiobacillus neapolitanus grown in continuous culture. — J. Gen. Microbiol., 126: 337–346.
Beudeker, R. F., Riegman, R. and Kuenen, J. G. 1981d. Regulation of nitrogen assimilation by the obligate chemolithotroph Thiobacillus neapolitanus. — J. Gen. Microbiol., in press.
Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254.
Cohen, Y., de Jonge, I. and Kuenen, J. G. 1979. Excretion of glycollate by Thiobacillus neapolitanus in continuous culture. — Arch. Microbiol. 122: 189–194.
Friedrich, C. G. and Mitrenga, G. 1981. Oxidation of thiosulfate by Paracoccus denitrificans and other hydrogen bacteria. — FEMS Microbiol. Lett. 10: 209–212.
Goa, J. 1953. A microbiuret method for protein determination of total protein in cerebrospinal fluid. — Scand. J. Clin. Lab. Invest. 5: 218.
Gottschal, J. C. and Kuenen, J. G. 1980a. Mixotrophic growth of Thiobacillus A2 on acetate and thiosulfate as growth limiting substrates in the chemostat. — Arch. Microbiol. 126: 33–42.
Gottschal, J. C. and Kuenen, J. G. 1980b. Selective enrichment of facultatively chemolithotrophic thiobacilli and related organisms in continuous culture. — FEMS Microbiol. Lett. 7: 241–247.
Gottschal, J. C., Nanninga, H. and Kuenen, J. G. 1981a. Growth of Thiobacillus A2 under alternating growth conditions in the chemostat. — J. Gen. Microbiol. 126: 85–96.
Gottschal, J. C., Pol, A. and Kuenen, J. G. 1981b. Metabolic flexibility of Thiobacillus A2 during substrate transitions in the chemostat. — Arch. Microbiol. 129: 23–28.
Gottschal, J. C., de Vries, S. and Kuenen, J. G. 1979. Competition between the facultatively chemolithotrophic Thiobacillus A2, an obligately chemolitrophic Thiobacillus and a heterotrophic Spirillum for inorganic and organic substrates. — Arch. Microbiol. 121: 241–249.
Harder, W. and Veldkamp, H. 1968. Physiology of an obligately psychrophylic marine Pseudomonas species. — J. Appl. Bacteriol. 31: 12–23.
Kämpf, C. and Pfennig, N. 1980. Capacity of Chromatiaceae for chemotrophic growth. Specific respiration rates of Thiocystis violacea and Chromatium vinosum. — Arch. Microbiol. 127: 125–137.
Kuenen, J. G. 1975. Colourless sulfur bacteria and their role in the sulfur cycle. — Plant Soil 43: 49–76.
Kuenen, J. G. 1979. Growth yields and maintenance energy requirements in Thiobacillus species under energy limitation. — Arch. Microbiol. 122: 183–188.
Kuenen, J. G. and Veldkamp, H. 1972. Thiomicrospira pelophila gen. n. sp. n., a new obligately chemolithotrophic colourless sulfur bacterium. — Antonie van Leeuwenhoek 38: 241–256.
Kuenen, J. G. and Veldkamp, H. 1973. Effects of organic compounds on chemostat cultures of Thiomicrospira pelophila, Thiobacillus thioparus and Thiobacillus neapolitanus. — Arch. Microbiol. 94: 173–190.
Matin, A. 1978. Organic nutrition of chemolithotrophic bacteria. — Annu. Rev. Microbiol. 32: 433–469.
Munro, H. N. and Fleck, A. 1966. The determination of nucleic acids. — Meth. Biochem. Anal. 14: 113–176.
Orion Research Incorporated. 1979. Instruction manual sulfide ion electrode and silver ion electrode model 94-16. Cambridge (Mass.) USA.
Rittenberg, S. C. 1969. The role of exogenous matter in the physiology of chemolithotrophic bacteria. — Adv. Microb. Physiol. 3: 159–195.
Smith, A. J. and Hoare, D. S. 1977. Specialist phototrophs, lithotrophs and methylotrophs: a unity among a diversity of prokaryotes? — Bacteriol. Rev. 41: 419–448.
Smith, A. L., Kelly, D. P. and Wood, A. P. 1980. Metabolism of Thiobacillus A2 grown under autotrophic, mixotrophic and heterotrophic conditions in chemostat culture. — J. Gen. Microbiol. 121: 127–138.
Sörbo, B. 1957. A colorimetric method for the determination of thiosulfate. — Biochim. Biophys. Acta 23: 412–416.
Tuttle, J. H. and Jannasch, H. W. 1972. Occurrence and types of thiobacillus-like bacteria in the sea. — Limnol. Oceanogr. 17: 523–543.
Vishniac, W. and Santer, M. 1957. The thiobacilli. — Bacteriol. Rev. 21: 195–213.
Wood, A. P. and Kelly, D. P. 1980. Carbohydrate degradation pathways in Thiobacillus A2 grown on various sugars. — J. Gen. Microbiol. 120: 333–345.
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Beudeker, R.F., Gottschal, J.C. & Kuenen, J.G. Reactivity versus flexibility in thiobacilli. Antonie van Leeuwenhoek 48, 39–51 (1982). https://doi.org/10.1007/BF00399485
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DOI: https://doi.org/10.1007/BF00399485