Plant and Soil

, Volume 43, Issue 1–3, pp 49–76 | Cite as

Colourless sulfur bacteria and their role in the sulfur cycle

  • J. Gijs Kuenen


The bacteria belonging to the families of the Thiobacteriaceae, Beggiatoaceae and Achromatiaceae are commonly called the colourless sulfur bacteria. While their ability to oxidize reduced inorganic sulfur compounds has clearly been established, it is still not known whether all these organisms can derive metabolically useful energy from these oxidations.

During the last decades research has mainly focussed on the genus Thiobacillus. Bacteria belonging to this genus can oxidize a variety of reduced inorganic sulfur compounds and detailed information is available on the biochemistry and physiology of these energy-yielding reactions. The thiobacilli, most of which can synthesize all cell material from CO2, possess a well-regulated metabolic machinery with high biosynthetic capacities, which is essentially similar to that of other procaryotic organisms.

Although the qualitative role of colourless sulfur bacteria in the sulfur cycle is well documented, quantitative data are virtually absent. Activities of colourless sulfur bacteria in nature must be related to direct and indirect parameters, such as: the rate of oxidation of (S35) sulfur compounds, the rate of C14O2-fixation, the rate of acid production and numbers and growth rates of the bacteria. However, chemical reactions and similar activities of heterotrophic organisms mask the activities of the colourless sulfur bacteria to various extents, depending on the condition of the natural environment. This interference is minimal in regions where high temperature and/or low pH allow the development of a dominant population of colourless sulfur bacteria, such as hot acid sulfur springs, sulfide ores, sulfur deposits and some acid soils.

The oxidation of inorganic sulfur compounds is carried out by a spectrum of sulfur-oxidizing organisms which includes: 1) obligately chemolithotrophic organisms 2) mixotrophs 3) chemolithotrophic heterotrophs 4) heterotrophs which do not gain energy from the oxidation of sulfur compounds but benefit in other ways from this reaction, and 5) heterotrophs which do not benefit from the oxidation of sulfur compounds. The spectrum is completed by a hypothetical group of heterotrophic organisms, which may have a symbiotic relationship with thiobacilli and related bacteria. Such heterotrophs may stimulate the growth of colourless sulfur bacteria and thereby contribute to the oxidation of sulfur compounds.

Future research should focus in the first place on obtaining and studying pure cultures of many of the colourless sulfur bacteria. In the second place, studies on the physiological and ecological aspects of mixed cultures of colourless sulfur bacteria and heterotrophs may add to a better understanding of the role of the colourless sulfur bacteria in the sulfur cycle.


Sulfur Compound Thiobacillus Sulfur Deposit Sulfur Cycle Heterotrophic Organism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Attoe, O. J. and Olsen, R. A., Factors affecting rate of oxidation in soils of elemental sulfur and that added in rock phosphate-sulfur fusions. Soil Sci.101, 317–325 (1966).Google Scholar
  2. 2.
    Baalsrud, K. and Baalsrud, K. S., Studies onThiobacillus denitrificans. Arch. Mikrobiol.20, 34–62 (1954).CrossRefPubMedGoogle Scholar
  3. 3.
    Bavendamm, W., Die farblosen und roten Schwefelbakterien.In Pflanzenforschung, Heft 2, pp. 1–157. (Ed. R. Kolkwitz) Gustav Fischer Verlag, Jena (1924).Google Scholar
  4. 4.
    Belly, R. T. and Brock, T. D., Ecology of iron oxidizing bacteria in pyrite materials associated with coal. J. Bacteriol.117, 726–732 (1974).PubMedGoogle Scholar
  5. 5.
    Bloomfield, C., The oxidation of iron sulphides in soils in relation to the formation of acid sulphate soils, and of ochre deposits in field drains. J. Soil Sci.23, 1–16 (1972).Google Scholar
  6. 6.
    Boer, W. E. de, Rivière, J. W. M. la, and Schmidt, K., Some properties ofAchromatium oxaliferum. Antonie van Leeuwenhoek J. Microbiol. Serol.37, 553–563 (1971).CrossRefGoogle Scholar
  7. 7.
    Borichewski, R. M., Keto acids as growth-limiting factors in autotrophic growth ofThiobacillus thiooxidans. J. Bacteriol.93, 597–599 (1967).PubMedGoogle Scholar
  8. 8.
    Borichewski, R. M. and Umbreit, W. W., Growth ofThiobacillus thiooxidans on glucose. Arch. Biochem. Biophys.116, 97–102 (1966).CrossRefPubMedGoogle Scholar
  9. 9.
    Brock, T. D., Principles of microbial ecology, Prentice-Hall Inc., Englewood Cliffs, New Jersey (1966).Google Scholar
  10. 10.
    Brock, T. D., Brock, M. L., Bott, T. L., and Edwards, M. R., Microbial life at 90°C; the sulfur bacteria of Boulder springs. J. Bacteriol.107, 303–314 (1971).PubMedGoogle Scholar
  11. 11.
    Brock, T. D., Brock, K. M., Belly, R. T. and Weiss, R. L., Sulfolobus: A new genus of sulfur oxidizing bacterial living at low pH, and high temperature. Arch. Mikrobiol.84, 54–68 (1972).CrossRefPubMedGoogle Scholar
  12. 12.
    Buchanan, R. E.,In Bergey's Manual of Determinative Bacteriology, 7th Ed., pp. 837–844. (Eds. R. S. Breed, E. G. D. Murray and N. R. Smith.) The Williams and Wilkins Comp., Baltimore (1957).Google Scholar
  13. 13.
    Burns, G. R., Oxidation of sulphur in soils. The Sulphur Institute, Washington and London, Technical Bulletin No. 13, pp. 1–41 (1967).Google Scholar
  14. 14.
    Burton, S. D. and Morita, R. Y., Effect of catalase and cultural conditions on growth ofBeggiatoa. J. Bacteriol.88, 1755–1761 (1964).PubMedGoogle Scholar
  15. 15.
    Caldwell, D. E. and Caldwell, S. J., The response of littoral communities of bacteria to variations in sulfide and thiosulfate. Bacteriol. Proc. G239 (1974).Google Scholar
  16. 16.
    Charles, A. M. and Suzuki, I., Sulfite oxidase of a facultative autotroph,Thiobacillus novellus. Biochem. Biophys. Research Commun.19, 686–690 (1965).Google Scholar
  17. 17.
    Chen, K. Y. and Morris, J. C., Oxidation of aqueous sulfide by O2:1. general characteristics and catalytic influences.In Adv. in Water Pollution Research,11, pp. 111-32/17–111-32/16 (Ed. S. H. Jenkins) Pergamon Press, San Francisco (1972).Google Scholar
  18. 18.
    Chen, K. Y. and Morris, J. C., Kinetics of oxidation of aqueous sulfide by O2. Environm. Sci. Technol.6, 529–537 (1972).Google Scholar
  19. 19.
    Cline, J. D. and Richards, F. A., Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature and pH. Environm. Sci. Technol.3, 838–843 (1969).Google Scholar
  20. 20.
    Collins, V. G., Isolation, cultivation and maintenance of autotrophs.In Methods in Microbiology,3B, pp. 1–52. (Ed. J. R. Norris and D. W. Ribbons) Academic Press, London, New York (1969).Google Scholar
  21. 21.
    Cornish, A. S. and Johnson, E. J., Regulation of pyruvate kinase fromThiobacillus neapolitanus. Arch. Biochem. Biophys.142, 584–590 (1971).CrossRefPubMedGoogle Scholar
  22. 22.
    Farquhar, G. J. and Boyle, W. C., Control of Thiothrix in activated sludge. J. Water Pollution Control Fed.44, 14–24 (1972).Google Scholar
  23. 23.
    Faust, L. and Wolfe, R. S., Enrichment and cultivation ofBeggiatoa alba. J. Bacteriol.81, 99–106 (1961).PubMedGoogle Scholar
  24. 24.
    Fliermans, C. B. and Brock, T. D., Ecology of sulfur-oxidizing bacteria in hot acid soils. J. Bacteriol.111, 343–350 (1972).PubMedGoogle Scholar
  25. 25.
    Gleen, H. and Quastel, J. H., Sulphur metabolism in soil. Appl. Microbiol.1, 70–77 (1953).PubMedGoogle Scholar
  26. 26.
    Guitonneau, G. and Keiling, J., L'évolution et la solubilisation du soufre élémentaire dans la terre arable. Ann. agron. NS2, 690–725 (1932).Google Scholar
  27. 27.
    Hampton, M. L. and Hanson, R. S., Regulation of isocitrate dehydrogenase fromThiobacillus thiooxidans andPseudomonas fluorescens. Biochem. Biophys. Research Commun.36, 296–305 (1969).Google Scholar
  28. 28.
    Hansen, T. A., Sulfide als electrondonor voor Rhodospirillaceae. Dissertation, University of Groningen (1974).Google Scholar
  29. 29.
    Hart, M. G., Sulphur oxidation in tidal mangrove soils of Sierra Leone. Plant and Soil11, 215–236 (1959).CrossRefGoogle Scholar
  30. 30.
    Hinze, G., Beitrage zur Kenntnis der farblosen Schwefelbakterien. Ber. Deutsch. Bot. Ges.31, 189–202 (1913).Google Scholar
  31. 31.
    Howard, R. and Stanier, R. Y., The genera Leucothrix and Thiothrix. Bacteriol. Rev.19, 49–64 (1955).Google Scholar
  32. 32.
    Hutchinson, M., Johnstone, K. I. and White, D., Taxonomy of the genus Thiobacillus: the outcome of numerical taxonomy applied to the group as a whole. J. Gen. Microbiol.57, 397–410 (1969).PubMedGoogle Scholar
  33. 33.
    Janke, A. and Breed, R. S.,In Bergey's Manual of determinative bacteriology, 7th Ed., pp. 78–88, 83–84 (Eds. R. S. Breed, E. G. D. Murray and N. R. Smith) The Williams and Wilkins Comp., Baltimore (1957).Google Scholar
  34. 34.
    Jannasch, H. W., Enrichment of aquatic bacteria in continuous culture. Arch. Mikrobiol.59, 165–173 (1967).CrossRefPubMedGoogle Scholar
  35. 35.
    Jørgensen, B. B. and Fenchel, T., The sulfur cycle of a marine sediment model system. Marine Biology24, 189–201 (1974).CrossRefGoogle Scholar
  36. 36.
    Johnson, C. and Vishniac, W., Chemoautotrophic bacteria.In Handbook of Microbiology, pp. 5–15 (Eds. A. I. Laskin and H. A. Lechevalier) CRC Press, Cleveland (1972).Google Scholar
  37. 37.
    Karavaiko, G. I. and Pivovarova, T. A., Oxidation of elemental sulfur byThiobacillus thiooxidans. Mikrobiologiya42, 345–350 (1973) (Engl. transl.).Google Scholar
  38. 38.
    Karavaiko, G. I., Shchetinina, E. V., Pivovarova, T. A. and Mubarakova, K. Y., Denitrifying bacteria isolated from deposits of sulfide ores. Mikrobiologiya42, 109–114 (1973) (Engl. transl.).Google Scholar
  39. 39.
    Keil, F., Beitrage zur Physiologie der farblosen Schwefelbakterien. Beitr. Biol. Pflanz.11, 335–372 (1912).Google Scholar
  40. 40.
    Kelly, D. P., The incorporation of acetate by the chemoautotrophThiobacillus neapolitanus strain C. Arch. Mikrobiol.58, 99–116 (1967).CrossRefPubMedGoogle Scholar
  41. 41.
    Kelly, D. P., Autotrophy: Concepts of lithotrophic bacteria and their organic metabolism. Ann. Rev. Microbiol.25, 177–210 (1971).Google Scholar
  42. 42.
    Kelly, D. P., Transformations of sulphur and its compounds in soils. Intern. Symp. Sulphur in Agriculture (1970). Annale agronomique, Numéro hors série 217–232 (1972).Google Scholar
  43. 43.
    Kelly, D. P. and Tuovinen, O. H., Recommendation that the namesFerrobacillus ferrooxidans Leathen and Braley andF. sulfoxidans Kinsel be recognized as synonyms ofThiobacillus ferrooxidans Temple and Colmer. Intern. J. Syst. Bacteriol.22, 170–172 (1972).Google Scholar
  44. 44.
    Kowalik, U. and Pringsheim, E. G., The oxidation of hydrogen sulfide by Beggiatoa. Am. J. Botany53, 801–806 (1966).Google Scholar
  45. 45.
    Kuenen, J. G., Een studie van kleurloze zwavelbacteriën uit het Groninger Wad. Dissertation, University of Groningen (1972).Google Scholar
  46. 46.
    Kuenen, J. G., unpublished results.Google Scholar
  47. 47.
    Kuenen, J. G. and Veldkamp, H.,Thiomicrospira pelophila, nov. gen., nov. sp., a new obligately chemolithotrophic colourless sulfur bacterium. Antonie van Leeuwenhoek J. Microbiol. Serol.38, 241–256 (1972).CrossRefGoogle Scholar
  48. 48.
    Kuenen, J. G. and Veldkamp, H., Effects of organic compounds on growth of chemostat cultures ofThiomicrospira pelophila, Thiobacillus thioparus andThiobacillus neapolitanus. Arch. Mikrobiol.94, 173–190 (1973).CrossRefPubMedGoogle Scholar
  49. 49.
    Kuznetsov, S. I., Die Rolle der Mikroorganismen im Stoffkreislauf der Seen. (Transl. 1959) (Ed. A. Pochman) VEB Deutscher Verlag der Wissenschaften, Berlin (1952).Google Scholar
  50. 50.
    Kuznetsov, S. I. and Sokolova, G. A., Contributions to the physiology ofThiobacillus thioparus. Mikrobiologiya29, 131–134 (1960) (Engl. transl.).Google Scholar
  51. 51.
    Léjohn, H. B., Van Caeseele, L. and Lees, H., Catabolite repression in the facultative chemoautotrophThiobacillus novellus. J. Bacteriol.94, 1484–1491 (1967).PubMedGoogle Scholar
  52. 52.
    London, J.,Thiobacillus intermedius nov. sp. A novel type of facultative autotroph. Arch. Mikrobiol.46, 329–337 (1963).CrossRefGoogle Scholar
  53. 53.
    London, J. and Rittenberg, S. C.,Thiobacillus perometabolis nov. sp., a non autotrophic Thiobacillus. Arch. Mikrobiol.59, 218–225 (1967).CrossRefPubMedGoogle Scholar
  54. 54.
    Matin A. and Rittenberg, S. C., Regulation of glucose metabolism inThiobacillus intermedius. J. Bacteriol.104, 239–246 (1970).PubMedGoogle Scholar
  55. 55.
    Matin, A. and Rittenberg, S. C., Enzymes of carbohydrate metabolism inThiobacillus species. J. Bacteriol.107, 179–186 (1971).PubMedGoogle Scholar
  56. 56.
    Mosser, J. L., Mosser, A. G., and Brock, T. D., Growth rates ofSulfolobus acidocaldarius in nature. J. Bacteriol.118, 1075–1081 (1974).PubMedGoogle Scholar
  57. 58.
    Niemelä, S. I. and Tuovinen, O. H., Acidophilic Thiobacilli in the River Sirppujoki. J. Gen. Microbiol.73, 23–28 (1972).Google Scholar
  58. 59.
    Pan, P. C. and Umbreit, W. W., Growth of obligate autotrophic bacteria on glucose in a continuous flow-through apparatus. J. Bacteriol.109, 1149–1155 (1972).PubMedGoogle Scholar
  59. 60.
    Pan, P. C. and Umbreit, W. W., Growth of mixed cultures of autotrophic and heterotrophic organisms. Can J. Microbiol.18, 153–156 (1972).PubMedGoogle Scholar
  60. 61.
    Pearce, J., Leach, C. K. and Carr, N. G., The incomplete tricarboxylic acid cycle in the blue-green algaAnabaena variabilis. J. Gen Microbiol.55, 371–378 (1969).PubMedGoogle Scholar
  61. 62.
    Peeters, T., Liu, M. S. and Aleem, M. I. H., The tricarboxylic acid cycle inThiobacillus denitrificans andThiobacillus A2. J. Gen. Microbiol.64, 29–35 (1970).PubMedGoogle Scholar
  62. 63.
    Peck, H. D., Symposium on metabolism of inorganic compounds. V. Comparative metabolism of inorganic sulfur compounds in microorganisms. Bacteriol. Rev.26, 67–94 (1962).PubMedGoogle Scholar
  63. 64.
    Quayle, J. R., The metabolism of one carbon compounds. Adv. Microbiol. Physiol.7, 119–203 (1972).Google Scholar
  64. 65.
    Quispel, A., Harmsen, G. W. and Otzen, D., Contribution to the chemical and bacteriological oxidation of pyrite in soil. Plant and Soil4, 43–55 (1952).CrossRefGoogle Scholar
  65. 66.
    Rittenberg, S. C., The roles of exogenous organic matter in the physiology of chemolithotrophic bacteria. Adv. Micr. Physiol.3, 159–196 (1969).Google Scholar
  66. 67.
    Rittenberg, S. C., The obligate autotroph — the demise of a concept. Antonie van Leeuwenhoek, J. Microbiol. Serol.38, 457–478 (1972).Google Scholar
  67. 68.
    Rivière, J. W. M. la, Enrichment of colourless sulfur bacteria. Zbl. Bakt. Abt. I., Orig. Suppl.1, 17–27 (1965).Google Scholar
  68. 69.
    Rivière, J. W. M. la, The microbial sulfur cycle and some of its implications for the geochemistry of sulfur isotopes. Geolog. Rundschau55, 568–582 (1966).Google Scholar
  69. 70.
    Roy, A. B. and Trudinger, P. A., The biochemistry of inorganic compounds of sulphur. Cambridge University Press, London, New York (1970).Google Scholar
  70. 71.
    Scotten, H. L. and Stokes, J. L., Isolation and properties of Beggiatoa. Arch. Mikrobiol.42, 353–368 (1962).CrossRefGoogle Scholar
  71. 72.
    Shafia, F. and Wilkinson, R. F., Growth ofFerrobacillus ferrooxidans on organic matter. J. Bacteriol.97, 256–260 (1969).PubMedGoogle Scholar
  72. 73.
    Shively, J. M., Ball, F., Brown, D. H. and Saunders, R. E., Functional organelles in prokaryotes. Science182, 584–586 (1973).PubMedGoogle Scholar
  73. 74.
    Smith, A. J., London, J., and Stanier, R. Y., Biochemical basis of obligate autotrophy in blue-green algae and thiobacilli. J. Bacteriol.94, 972–983 (1967).PubMedGoogle Scholar
  74. 75.
    Sokolova, G. A. and Karavaiko, G. I., Physiology and geochemical activity of Thiobacilli. Israel Programme for Scientific Translations, Jerusalem (1968).Google Scholar
  75. 76.
    Sorokin, Y. I., The mechanism of chemical and biological oxidation of sodium, calcium and iron sulfides. Mikrobiologiya39, 220–224 (1970) (Engl. transl.).Google Scholar
  76. 77.
    Sorokin, Y. I., The bacterial population and the process of hydrogen sulfide oxidation in the Black Sea. J. Cons. Intern. Explor. Mer34, 423–454 (1972).Google Scholar
  77. 78.
    Sorokin, Y. I. and Kadota, H., Techniques for the assessment of microbial production and decomposition in fresh water. IBP Handbook23 (1972).Google Scholar
  78. 79.
    Starkey, R. L., Isolation of some bacteria which oxidize thiosulfate. Soil Sci.39, 197–219 (1935).Google Scholar
  79. 80.
    Starkey, R. L., Oxidation and reduction of sulfur compounds in soils. Soil Sci.101, 297–306 (1966).Google Scholar
  80. 81.
    Taylor, B. F., Regulation of citrate synthase activity in strictly and facultatively autotrophic thiobacilli. Biochem. Biophys. Research Commun.40, 957–963 (1970).Google Scholar
  81. 82.
    Taylor, B. F. and Hoare, D. S., New facultative Thiobacillus and a reevaluation of the heterotrophic potential ofThiobacillus novellus. J. Bacteriol.100, 487–497 (1969).PubMedGoogle Scholar
  82. 83.
    Taylor, B. F. and Hoare, D. S.,Thiobacillus denitrificans as an obligate chemolithotroph. II. Cell suspensions and enzymic studies. Arch. Mikrobiol.80, 262–276 (1971).CrossRefPubMedGoogle Scholar
  83. 84.
    Taylor, B. F., Hoare, D. S., and Hoare, S. L.,Thiobacillus denitrificans as an obligate chemolithotroph. Isolation and growth studies. Arch. Mikrobiol.78, 193–204 (1971).CrossRefPubMedGoogle Scholar
  84. 85.
    Tredway, J. V. and Burton, S. D., Morphological examination of Beggiatoa and Thiothrix obtained from bacterial mats on the surface of solid waste bales deposited in the continental shelf. Bacteriol. Proc. G105 (1974).Google Scholar
  85. 86.
    Trudinger, P. A., Metabolism of thiosulfate and tetrathionate by heterotrophic bacteria from soil. J. Bacteriol.93, 550–559 (1967).PubMedGoogle Scholar
  86. 87.
    Trudinger, P. A., The metabolism of inorganic sulphur compounds by thiobacilli. Rev. Pure and Appl. Chem.17, 1–24 (1967).Google Scholar
  87. 88.
    Tuovinen, O. H. and Kelly, D. P., Biology ofThiobacillus ferrooxidans in relation to the microbiological leaching of sulphide ores. Z. allg. Mikrobiol.12, 311–346 (1973).Google Scholar
  88. 89.
    Tuovinen, O. H. and 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).CrossRefPubMedGoogle Scholar
  89. 90.
    Tuttle, J. H., Dugen, P. R., MacMillan, C. B. and Randles, C. I., Microbial dissimilatory sulfur cycle in acid mine water. J. Bacteriol.97, 594–602 (1969).PubMedGoogle Scholar
  90. 91.
    Tuttle, J. H. and Jannasch, H. W., Occurrence and types of Thiobacillus-like bacteria in the sea. Limnol. Oceanogr.17, 532–543 (1972).Google Scholar
  91. 92.
    Tuttle, J. H. and Jannasch, H. W., Sulfide and thiosulfate-oxidizing bacteria in anoxic marine basins. Marine Biol.20, 64–70 (1973).CrossRefGoogle Scholar
  92. 93.
    Tuttle, J. H., Holmes, P. E. and Jannasch, H. W., Growth stimulation of marine pseudomonas by thiosulfate. Bacteriol. Proc. G238 (1974).Google Scholar
  93. 94.
    Tuttle, J. H., Holmes, P. E. and Jannasch, H. W., Growth rate stimulation of marine pseudomonads by thiosulfate. Arch. Mikrobiol.99, 1–14 (1974).Google Scholar
  94. 95.
    Vishniac, W. and Santer, M., The thiobacilli. Bacteriol. Rev.21, 195–213 (1957).Google Scholar
  95. 96.
    Vitolins, M. I. and Swaby, R. J., Activity of sulphur oxidizing micro-organisms in some Australian soils. Australian J. Soil Research7, 171–183 (1969).Google Scholar
  96. 97.
    Water Pollution Research, Technical paper no. 11. Dep. of Scientific and Industrial Res., H. M. Stationery Office, London, pp. 188–194, 247–277 (1964).Google Scholar
  97. 98.
    Williams, R. A. D. and Hoare, D. S., Physiology of a new facultatively autotrophic thermophilic Thiobacillus, J. Gen. Microbiol.50, 555–566 (1972).Google Scholar
  98. 99.
    Winogradski, S., Contribution à la morphologie et à la physiologie des sulfobactéries (1888).In Microbiologie du Sol, Oeuvres Complètes, Massón et Cie., Paris, pp. 83–126 (1949).Google Scholar
  99. 100.
    Wirsen, C. O., Gonye, E. R., and Jannasch, H. W., Physiological and morphological studies on Thiovulum sps. Bacteriol. Proc. G237 (1974).Google Scholar
  100. 101.
    Woolley, D., Jones, G. L., and Happold, F. C., Some metabolic differences betweenThiobacillus thioparus, T. denitrificans andT. thiocyanooxidans. J. Gen. Microbiol.29, 311–316 (1962).PubMedGoogle Scholar
  101. 102.
    Zajic, J. E., Microbial biogeochemistry. Academic Press, New York, London (1969).Google Scholar
  102. 103.
    Zavarzin, G. A. and Zhilina, T. N., Thione bacteria from thermal springs. Mikrobiologiya33, 753–758 (1964) (Engl. transl.).Google Scholar

Copyright information

© Martinus Nijhoff 1975

Authors and Affiliations

  • J. Gijs Kuenen
    • 1
  1. 1.Laboratory of MicrobiologyUniversity of Groningen, Biological CentreHaren (Gr.)The Netherlands

Personalised recommendations