Surface Structures of New and Lesser Known Species of Thermobifida as Revealed by Scanning Electron Microscopy

Abstract

Surface structures of representatives of the genus Thermobifida were examined by scanning electron microscopy. Spores formed at the tips of multibranched sporophores initially resembled short sausages; then, upon maturation, they gradually built up their typical ovoid shape. Characteristic differences were observed between T. cellulolytica strain TB108 and T. fusca strains TM51. The spores of TB108 were larger (0.8×1.3 μm) than those of TM51 (0.6×1.1 μm) in consequence of the more thickened outer squamous layer. When Thermobifida strains were grown on cellulose as sole carbon source, the mycelium was found to coil around the cellulose crystals and multiple protuberances emerged, resulting in a scabrous appearance to the mycelial surface. The presence of these cellulosome-like structures yielded a 24.5% surface enlargement of the scabrous mycelium as compared with the smooth one. The cellulosome emergence pattern paralleled the proportional increase in free endoglucanase activity measured during the culturing of these actinomycetes in the presence of cellulose.

References

  1. 1.

    Bayer E. A., Lamed, R. (1986) Ultrastructure of the cell surface cellulosome of Clostridium ther-mocellum and its interaction with cellulose. J. Bacteriol. 167, 828–836.

    CAS  Article  Google Scholar 

  2. 2.

    Blanco J., Coque J. J., Velasco J., Martin, J. F. (1997) Cloning, expression in Streptomyces lividans and biochemical characterization of a thermostable endo-beta-1,4-xylanase of Thermomonospora alba ULJB1 with cellulose-binding ability. Appl. Microbiol. Biotechnol. 48, 208–217.

    CAS  Article  Google Scholar 

  3. 3.

    Bozzola J. J., Russel, L. D. (1992) Specimen preparation for scanning electron microscopy. In: J. J. Bozzola, L. D. Russel (eds) Electron Microscopy. Jones and Bartlett Publishers, London, pp. 40–64.

    Google Scholar 

  4. 4.

    Crawford D. L., Gonda, M. A. (1977) The sporulation process in Thermomonospora fusca as revealed by scanning and transmission electron microscopy. Can. J. Microbiol. 23, 1088–1095.

    CAS  Article  Google Scholar 

  5. 5.

    Henssen, A. (1957) Beitrage zur morphologie und systematik der thermophilen actinomyceten. Arch. Microbiol. 26, 373–414.

    CAS  Google Scholar 

  6. 6.

    Hostalka F., Moultrie A., Stutzenberger, F. (1992) Influence of carbon source on cell surface topology of Thermomonospora curvata. J. Bacteriol. 174, 7048–7052.

    CAS  Article  Google Scholar 

  7. 7.

    Kleeberg I., Hetz, C., Kroppenstedt R. M., Muller R. J., Deckwer, W. D. (1998) Biodegradation of aliphatic-aromatic copolyesters by Thermomonospora fusca and other thermophilic compost isolates. Appl. Environ. Microbiol. 64, 1731–1735.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Kukolya J., Dobolyi, C., Hornok, L. (1997) Isolation and identification of thermophilic cellulolytic actinomycetes. Acta Phytopath. Entomol. Hung. 32, 97–107.

    Google Scholar 

  9. 9.

    Kukolya J., Laday M., Halbritter A., Oravecz O., Marialigeti K., Hornok, L. (2000) Thermobifida cellulolytica sp. nov., a new lignocellulose decomposing member of the genus Thermobifida. Proceedings of the General Assembly of the Hungarian Society for Microbiology, Keszthely, 63 p.

    Google Scholar 

  10. 10.

    Lamed R., Naimark J., Morgenstern E., Bayer, E. A. (1987) Specialized cell surface structures in cellulolytic bacteria. J. Bacteriol. 169, 3792–3800.

    CAS  Article  Google Scholar 

  11. 11.

    Lao G., Gurdev S., Ghangas G. S., Jung E. D., Wilson, D. B. (1991) DNA sequences of three p-1,4-endoglucanase genes from Thermomonospora fusca. J. Bacteriol. 173, 3397–3407.

    CAS  Article  Google Scholar 

  12. 12.

    McCarthy, A. J. (1989) Thermomonospora and related genera. In: S. T. Williams, M. E. Sharpe, J. G. Holt (ed.) Bergey’ s Manual of Systematic Bacteriology, Vol. 4. Williams and Wilkins, Baltimore, pp. 2552–2572.

    Google Scholar 

  13. 13.

    Schlochtermeier A., Niemeyer F., Schrempf, H. (1992) Biochemical and electron microscopic studies of the Streptomyces reticuli cellulase (avicelase) in its mycelium-associated and extracellular forms. Appl. Environ. Microbiol. 58, 3240–3248.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Spiridonov N. A., Wilson, D. B. (1998) Regulation of biosynthesis of individual cellulases in Thermomonospora fusca. J. Bacteriol. 180, 3529–3532.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Stutzenberger, F. J. (1991) Cellulose degradation by thermophilic aerobic bacteria. In: C. H. Haigler, P. J. Weimer (eds) Biosynthesis and Biodegradation of Cellulose. Marcel Dekker, New York, pp. 445–490.

    Google Scholar 

  16. 16.

    Walter S., Rohde M., Machner M., Schrempf, H. (1999) Electron microscopy studies of cell-wall-anchored cellulose (Avicel)-binding protein (AbpS) from Streptomyces reticuli. Appl. Environ. Microbiol. 65, 886–892.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Whitney, P. J. (1982) Cellulase and pectinase induction and estimation. In: S. B. Primrose, A. C. Wardlaw (eds) Sourcebook of Experiments for the Teaching of Microbiology. Academic Press, New York, pp. 626–630.

    Google Scholar 

  18. 18.

    Zhang Z., Wang, Y, Ruan, J. (1998) Reclassification of Thermomonospora and Microtetraspora. Int. J. Syst. Bacteriol. 48, 411–422.

    Article  Google Scholar 

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Correspondence to L. Hornok.

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Dedicated to Professor Lajos Ferenczy on the occasion of his 70th birthday.

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Kukolya, J., Szabó, L. & Hornok, L. Surface Structures of New and Lesser Known Species of Thermobifida as Revealed by Scanning Electron Microscopy. BIOLOGIA FUTURA 52, 211–221 (2001). https://doi.org/10.1556/ABiol.52.2001.2-3.5

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Keywords

  • Thermobifida
  • sporogenesis
  • scanning electron microscopy
  • cellulosome
  • endoglucanase activity