1887

Abstract

Streptomycetes belong to the ecologically important bacterial population within soil, which is also inhabited by many fungi. The highly chitinolytic and the ascomycete were chosen as models to test for interactions among bacteria and fungi. In medium lacking a soluble carbon source, individually cultivated spores of the bacterium and the fungus do not germinate. However, as shown by viability tests, cultivation of a mixture of both spore types provokes successive events: (i) stimulation of the germination of spores, (ii) initiation of the outgrowth of some fungal spores to which the chitinase ChiO1 adheres, (iii) massive extension of viable networks of hyphae at the expense of fungal hyphae and (iv) balanced proliferation of closely interacting fungal and hyphae. The replacement of the wild-type strain by a chromosomal disruption mutant (ΔC), lacking production of the extracellular chitin-binding protein CHB1 but still secreting the chitinase ChiO1, provokes (v) germination of each spore type, (vi) retarded development of both partners, followed by (vii) preferential proliferation of the fungus. Together with biochemical and immunomicroscopy studies, the data support the conclusion that CHB1 molecules aggregate to an extracellular matrix, maintaining a close contact, followed by several concerted responses of the bacterium and the fungus.

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2007-02-01
2020-04-08
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References

  1. Adams D. J.. 2004; Fungal cell wall chitinases and glucanases. Microbiology150:2029–2035[CrossRef]
    [Google Scholar]
  2. Beyer M., Diekmann H.. 1985; The chitinase system of Streptomyces sp. ATCC 11238 and its significance for fungal cell wall degradation. Appl Microbiol Biotechnol23:140–146[CrossRef]
    [Google Scholar]
  3. Blaak H., Schrempf H.. 1995; Binding and substrate specificities of a Streptomyces olivaceoviridis chitinase in comparison with its proteolytically processed form. Eur J Biochem229:132–139[CrossRef]
    [Google Scholar]
  4. Blaak H., Schnellmann J., Walter S., Henrissat B., Schrempf H.. 1993; Characteristics of an exochitinase from Streptomyces olivaceoviridis , its corresponding gene, putative protein domains and relationship to other chitinases. Eur J Biochem214:659–669[CrossRef]
    [Google Scholar]
  5. Chu H. H., Hoang V., Hofemeister J., Schrempf H.. 2001; A Bacillus amyloliquefaciens ChbB protein binds β - and α -chitin and has homologues in related strains. Microbiology147:1793–1803
    [Google Scholar]
  6. Fernandez M., Sanchez J.. 2002; Nuclease activities and cell death processes associated with the development of surface cultures of Streptomyces antibioticus ETH 7451. Microbiology148:405–412
    [Google Scholar]
  7. Fillinger S., Chaveroche M. K., Shimizu K., Keller N., d'Enfert C.. 2002; cAMP and ras signalling independently control spore germination in the filamentous fungus Aspergillus nidulans . Mol Microbiol44:1001–1016[CrossRef]
    [Google Scholar]
  8. Harrison M. J.. 2005; Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol59:19–24[CrossRef]
    [Google Scholar]
  9. Hopwood D. A., Bibb M. J., Chater K. F., Kieser T., Bruton C. J., Kieser H. M., Lydiate D. J., Smith C. P., Ward J. M., Schrempf H.. 1985; Genetic Manipulation of Streptomyces: a Laboratory Manual Norwich: John Innes Foundation;
    [Google Scholar]
  10. Klein D. A., Paschke M. W.. 2004; Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microb Ecol47:224–235
    [Google Scholar]
  11. Kutzner H. J.. 1981; The family Streptomycetaceae . In The Prokaryotes: a Handbook on Habitats, Isolation and Identification of Bacteria pp2028–2090 Edited by Starr M. P., Stolp H., Balows A., Schlegel H., Trüper H. G.. Berlin: Springer;
    [Google Scholar]
  12. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  13. Leal-Morales C. A., Bracker C. E., Bartnicki-Garcia S.. 1988; Localization of chitin synthetase in cell-free homogenates of Saccharomyces cerevisiae : chitosomes and plasma membrane. Proc Natl Acad Sci U S A85:8516–8520[CrossRef]
    [Google Scholar]
  14. Rigali S., Nothaft H., Noens E. E., Schlicht M., Colson S., Muller M., Joris B., Koerten H. K., Hopwood D. A.. other authors 2006; The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N -acetylglucosamine metabolism to the control of development. Mol Microbiol61:1237–1251[CrossRef]
    [Google Scholar]
  15. Saito A., Schrempf H.. 2004; Mutational analysis of the binding affinity and transport activity for N -acetylglucosamine of the novel ABC transporter Ngc in the chitin-degrader Streptomyces olivaceoviridis . Mol Genet Genomics271:545–553[CrossRef]
    [Google Scholar]
  16. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  17. Schnellmann J., Zeltins A., Blaak H., Schrempf H.. 1994; The novel lectin-like protein CHB1 is encoded by a chitin-inducible Streptomyces olivaceoviridis gene and binds specifically to crystalline α -chitin of fungi and other organisms. Mol Microbiol13:807–819[CrossRef]
    [Google Scholar]
  18. Susstrunk U., Pidoux J., Taubert S., Ullmann A., Thompson C. J.. 1998; Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor . Mol Microbiol30:33–46[CrossRef]
    [Google Scholar]
  19. Svergun D. I., Becirevic A., Schrempf H., Koch M. H. J., Grüber G.. 2000; Solution structure and conformational changes of the Streptomyces chitin-binding protein (CHB1. Biochemistry39:10677–10683[CrossRef]
    [Google Scholar]
  20. Umeyama T., Lee P. C., Horinouchi S.. 2002; Protein serine/threonine kinases in signal transduction for secondary metabolism and morphogenesis in Streptomyces . Appl Microbiol Biotechnol59:419–425[CrossRef]
    [Google Scholar]
  21. Vionis A., Niemeyer F., Karagouni A. D., Schrempf H.. 1996; Production and processing of a 59 kDa exochitinase during growth of Streptomyces lividans pCHIO12 in soil microcosms amended with crab or fungal chitin. Appl Environ Microbiol62:1774–1780
    [Google Scholar]
  22. Wang F., Xiao X., Saito A., Schrempf H.. 2002; Streptomyces olivaceoviridis possesses a phosphotransferase system that mediates specific, phosphoenolpyruvate-dependent uptake of N -acetylglucosamine. Mol Genet Genomics268:344–351[CrossRef]
    [Google Scholar]
  23. Xiao X., Wang F., Saito A., Majka J., Schrempf H., Schlösser A.. 2002; The novel Streptomyces olivaceoviridis ABC transporter Ngc mediates uptake of N -acetylglucosamine and N , N ′-diacetylchitobiose. Mol Genet Genomics267:429–439[CrossRef]
    [Google Scholar]
  24. Zeltins A., Schrempf H.. 1995; Visualization of α -chitin with a specific chitin-binding protein (CHB1) from Streptomyces olivaceoviridis . Anal Biochem231:287–294[CrossRef]
    [Google Scholar]
  25. Zeltins A., Schrempf H.. 1997; Specific interaction of the Streptomyces chitin-binding protein CHB1 with α -chitin: the role of individual tryptophan residues. Eur J Biochem246:557–564[CrossRef]
    [Google Scholar]
  26. Zuber S., Hynes M. J., Andrianopoulos A.. 2002; G-protein signaling mediates asexual development at 25 °C but has no effect on yeast-like growth at 37 °C in the dimorphic fungus Penicillium mameffei . Eukaryot Cell1:440–447[CrossRef]
    [Google Scholar]
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