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The ultrastructure of chemolithoautotrophic Gallionella ferruginea and Thiobacillus ferrooxidans as revealed by chemical fixation and freeze-etching

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Abstract

By using sodium thioglycolate to dissolve the high amount of excreted stalk material in axenic cultures of the chemolithoautotrophic iron bacterium Gallionella ferruginea, the ultrastructure of Gallionella cells from pure cell suspensions could be studied without any loss of viability or disturbance by dense ferric stalk fibers, and compared with Thiobacillus ferrooxidans, also grown chemolithoautotrophically with ferrous iron as energy source. Both organisms were chemically fixed or freeze-etched. Particular structural differences between these iron-bacteria could be ascertained. G. ferruginea possesses intracytoplasmic membranes and soluble d-ribulose-1,5-bisphosphate-carboxylase, whereas T. ferrooxidans contains carboxysomes but no intracytoplasmic membranes; Gallionella forms poly-β-hydroxybutyrate and glycogen as storage material; T. ferrooxidans produces only glycogen. Both organisms also differ from each other with respect to the freeze fracture behaviour of the cell envelope layers. Whereas the cells of T. ferrooxidans exhibit a characteristic double cleavage, exposing the plasmic fracture face and exoplasmic fracture face of the outer membrane and cytoplasmic membrane, the exceptionally thin multilayered cell envelope of G. ferruginea revealed a particularly intimate association between the layers, resulting in a visualisation of the supramolecular organisation of only the inner fracture face of the cytoplasmic membrane. The results are discussed predominantly in relation to the extremely distinct environments of both organisms.

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References

  • Balashova VV, Cherni NE (1970) Ultrastructure of Gallionella filamenta. Mikrobiologija 39:348–351

    Google Scholar 

  • Beudeker RF, Kuenen JG (1981) Carboxysomes. “Calvinosomes”? FEBS Lett 131:269–274

    Google Scholar 

  • Branton D, Bullivant S, Gilula NB, Karnovsky MT, Moor H, Mühlenthaler K, Northcote DH, Packer L, Satir B, Speth V, Staehlin LA, Steere RL, Weinstein RS (1975) Freeze-etching nomenclature. Science 190:54–56

    Google Scholar 

  • Cedergren B, Holme T (1959) On the glycogen in Escherichia coli B. Electron microscopy of ultrathin sections of cells. J Ultrastruct Res 3:70–73

    Google Scholar 

  • Cheng KJ, Hiromaka R, Roberts DWA, Costerton JW (1973) Cytoplasmic glycogen inclusions in cells of anaerobic Gram-negative rumen bacteria. Can J Microbiol 19:1501–1509

    Google Scholar 

  • Cohen-Bazire G, Kunisawa R (1963) The fine structure of Rhodospirillum rubrum. J Cell Biol 16:401–419

    Google Scholar 

  • Costerton JW, Ingram JM, Cheng KJ (1974) Structure and function of the cell envelope of Gram-negative bacteria. Bacteriol Rev 38:87–100

    Google Scholar 

  • Dispersio Jr, Deal SJ (1974) Identification of intracellular polysaccharide granules in the thin sections of Nocardia asteroides. J Gen Microbiol 83:349–358

    Google Scholar 

  • Gebauer A (1988) Nachweis und Quantifizierung des Autotrophiestoffwechsels von Gallionella ferruginea Ehrenberg. Thesis submitted to receive Phil. D. V., Braunschweig, pp 1–75

  • Gebauer A, Bowien B, Hanert HH (1984) Autotrophic enzymes of Gallionella ferruginea and comparison of in vivo activity of its RuBP-carboxylase to Thiobacillus ferrooxidans and Alcaligenes eutrophus. Abstr Ann Meet German Local Branch ASM, Osnabrück 47

  • Ghiorse WC (1984) Biology of iron- and manganese-depositing bacteria. Ann Rev Microbiol 38:515–550

    Google Scholar 

  • Glauert AM, Thornley MJ (1969) The topology of the bacterial cell wall. Ann Rev Microbiol 23:159–198

    Google Scholar 

  • Hanert HH (1970) Struktur und Wachstum von Gallionella ferruginea Ehrenberg am natürlichen Standort in den ersten 6 Stunden der Entwicklung. Arch Mikrobiol 75:10–24

    Google Scholar 

  • Hanert HH (1975) Entwicklung, Physiologie und Ökologie des Eisenbakteriums Gallionella ferruginea Ehrenberg — Beiträge zu einer Monographie. Habilitationsschrift, Faculty of Science, University of Braunschweig

  • Hanert HH (1981) The genus Gallionella. In: Starr M, Stolp H, Tröper HC, Balows A, Schlegel HG (eds) The prokaryotes, a handbook on habitats, isolation and identification of bacteria. Springer, Berlin Heidelberg New York, pp 509–515

    Google Scholar 

  • Harms H, Kroops HP, Martiny H, Wullenweber M (1981) d-Ribulose 1,5 biphosphate carboxysomes and polyhedral inclusion bodies in Nitrosomonas spec. Arch Microbiol 128:280–281

    Google Scholar 

  • Holt SC, Shively JM, Greenawalt JW (1974) Fine structure of selected species of the Genus Thiobacillus as revaled by chemical fixation and freeze-etching. Can J Microbiol 20:1347–1351

    Google Scholar 

  • Kellenberger E, Ryter A, Sechaud J (1958) Electron microscope study of DNA-containing plasma. II. Vegetative and mature phage DNA as compared with normal bacterial nucleoids in different physiological states. J Biophys Biochem Cytol 4:671–676

    Google Scholar 

  • Kran G, Schlote W, Schlegel HG (1963) Cytologische Untersuchung an Chromatium okenii perty. Naturwiss 50:728–730

    Google Scholar 

  • Mayer F (1986) Cytology and morphogenesis of bacteria. Gebr Bornträger, Berlin Stuttgart

    Google Scholar 

  • Mollenhauer HH (1965) Plastic embedding mixture for the use in electron microscopy. Stain Technol 39:111–114

    Google Scholar 

  • Murray RGE, Watson W (1965) Structure of Nitrocystis oceanus and comparison with Nitrosomonas and Nitrobacter. J Bacteriol 89:1594–1606

    Google Scholar 

  • Purohit K, McFadden BA, Shakh MM (1976) d-Ribulose-1,5-bisphosphate carboxylase and polyhedral inclusion bodies by Thiobacillus intermedius. J Bacteriol 172:516–522

    Google Scholar 

  • Remsen CC, Lundgren DG (1966) Electron microscopy of the cell envelope of Ferrobacillus ferrooxidans prepared by freeze etching and chemical fixation technique. J Bacteriol 92:1765–1771

    Google Scholar 

  • Remsen CC, Watson SW (1972) Freeze-etching of bacteria. Int Rev Cytol 33:253–296

    Google Scholar 

  • Reynolds DM, Laishley EJ, Costerton JW (1981) Physiological and ultrastructural characterization of a new acidophilic Thiobacillus species. Can J Microbiol 27:151–161

    Google Scholar 

  • Robertson JG, Lyttleton P, Williamson KH, Batt RD (1975) The effect of fixation procedures on the electron density of polysaccharide granules in Nocardia corallina. J Ultrastruct Res 52:321–332

    Google Scholar 

  • Silverman DG, Lundgren MP (1959) Studies of the chemolithotrophic iron bacterium Thiobacillus ferrooxidans. J Bacteriol 77:642–648

    Google Scholar 

  • Shively JM, Decker GL, Greenwalt JW (1970) Comparative ultrastructure of the Thiobacilli. J Bacteriol 102:616–627

    Google Scholar 

  • Shively JM, Ball F, Brown DH, Sauder RE (1973) Functional organelles of prokaroytes: Polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182:584–586

    Google Scholar 

  • Sleytr VB, Kocur M, Thornely M, Glauert AM (1973) A study by freeze-etching of the fine structure of Micrococcus radiodurans. Arch Microbiol 94:77–87

    Google Scholar 

  • Walther-Mauruschat A, Aragno M, Mayer F, Schlegel HG (1977) Micromorphology of Gram-negative Hydrogen bacteria. II. Cell envelope, membranes, and cytoplasmic inclusions. Arch Microbiol 114:101–110

    Google Scholar 

  • Westphal K, Bock E, Cannon GC, Shively JM (1979) Desoxyribonucleic acid in Nitrobacter carboxysomes. J Bacteriol 140:285–288

    Google Scholar 

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Lütters, S., Hanert, H.H. The ultrastructure of chemolithoautotrophic Gallionella ferruginea and Thiobacillus ferrooxidans as revealed by chemical fixation and freeze-etching. Arch. Microbiol. 151, 245–251 (1989). https://doi.org/10.1007/BF00413137

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  • DOI: https://doi.org/10.1007/BF00413137

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