Skip to main content
SpringerLink
Log in

Bacterial adhesion to different termite flagellates: Ultrastructural and functional evidence for distinct molecular attachment modes

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The attachment modes of rodlike ectobiotic bacteria to the surface of two different termite flagellates were studied.Devescovina glabra was covered by laterally attached bacteria. Treatment with chemicals that disturb hydrophobic interactions and solubilize proteins removed the ectobionts. Freeze-fracture and freeze-etching electron microscopy revealed rows of intramembrane particles that occurred exclusively along the attachment sites. The adhering Gram-negative bacteria possessed an S-layer (surface layer) composed of globular protein particles. The S-layer could be removed by protein-solubilizing chemicals, e.g., urea, as shown by ultrathin-section electron microscopy. Therefore, it seems plausible that the attachment was mediated by hydrophobic interactions between the flagellate's plasma membrane and the S-layer of the bacteria. The bacteria of the second flagellate,Joenia annectens, adhered by their tips. The attachment was extremely strong. Chemicals disturbing ionic or hydrophobic bindings or solubilizing proteins did not detach the ectobionts. Globular intramembrane protein particles were preferentially found in a ringlike array at the external fracture face of the flagellate's contact sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DIC:

differential interference contrast

EGTA:

ethylene glycol-bis(β-aminoethyl ether) N,N,N′,N′-tetraacetic acid

TEM:

transmission electron microscope

Tween:

20 polyoxyethylenesorbitan

References

  • Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1994) Molecular biology of the cell, 3rd edn. Garland Publishing, New York

    Google Scholar 

  • Ball GH (1969) Organisms living on and in protozoa. In: Chen T-T (ed) Research in protozoology, vol 3. Pergamon Press, New York, pp 565–718

    Google Scholar 

  • Beams HW, King RL, Tahmisian TN, Devine R (1960) Electron microscope studies onLophomonas striata with special reference to the nature and position of the striations. J Protozool 7: 91–101

    Google Scholar 

  • Bloodgood RA, Fitzharris TP (1976) Specific associations of prokaryotes with symbiotic flagellate protozoa from the hindgut of the termiteReticulitermes and the wood-eating roachCryptocercus. Cytobios 17: 103–122

    Google Scholar 

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

    Google Scholar 

  • Breznak JA (1975) Symbiotic relationships between termites and their intestinal microbiota. In: Jennings DH, Lee DL (eds) Symbiosis. Cambridge University Press, Cambridge, pp 559–580 (Symposia of the Society for Experimental Biology, vol 29)

    Google Scholar 

  • Christensen GD, Simpson WA, Beachey EH (1985) Adhesion of bacteria to animal tissues: complex mechanisms. In: Savage DC, Fletcher M (eds) Bacterial adhesion. Plenum, New York, pp 279–305

    Google Scholar 

  • Cleveland LR, Grimstone AV (1964) The fine structure of the flagellateMixotricha paradoxa and its associated micro-organisms. Proc R Soc Lond B Biol Sci 159: 668–686

    Google Scholar 

  • Costerton JW, Geesey GG, Chen K-J (1978) How bacteria stick. Sci Am 238: 86–95

    Google Scholar 

  • —, Marrie TJ, Cheng K-J (1985) Phenomena of bacterial adhesion. In: Savage DC, Fletcher M (eds) Bacterial adhesion. Plenum, New York, pp 3–43

    Google Scholar 

  • Courtney HS, Hasty DL, Ofek I (1990) Hydrophobicity of group A streptococci and its relationship to adhesion of streptococci to host cells. In: Doyle RJ, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, DC, pp 361–386

    Google Scholar 

  • Epstein SS, Bazylinski DA, Fowle WH (1998) Epibiotic bacteria on several ciliates from marine sediments. J Euk Microbiol 45: 64–70

    Google Scholar 

  • Esteban G, Finlay BJ (1994) A new genus of anaerobic scuticociliate with endosymbiotic methanogens and ectobiotic bacteria. Arch Protistenk 144: 350–356

    Google Scholar 

  • Fenchel T, Finlay BJ (1989)Kentrophoros: a mouthless ciliate with a symbiotic kitchen garden. Ophelia 30: 75–93

    Google Scholar 

  • Gibbons RJ (1980) Adhesion of bacteria to the surfaces of the mouth. In: Berkeley RCW, Lynch JM, Melling J, Rutter PR, Vincent B (eds) Adsorption of microorganisms to surfaces. Ellis Horwood, Chichester, pp 351–388

    Google Scholar 

  • Grassé P-P (1952) Traité de zoologie, vol 1, phylogénie protozoaires: généralités, flagellées. Masson et Cie Éditeurs, Libraires de l'Academie de Medécine, Paris

    Google Scholar 

  • Hancock IC (1991) Microbial cell surface architecture. In: Mozes N, Handley PS, Busscher HJ, Rouxhet PG (eds) Microbial cell surface analysis: structural and physicochemical methods. VCH, Weinheim, pp 21–59

    Google Scholar 

  • Hollande A, Valentin J (1969) Appareil de Golgi, pinocytose, lysosomes, mitochondries, bactéries symbiontiques, atractophores et pleuromitose chez les Hypermastigines du genreJoenia: affinités entre Joeniides et Trichomonadines. Protistologica 5: 39–86

    Google Scholar 

  • Kirby H (1941) Devescovinid flagellates of termites I: the genusDevescovina. Univ Calif Publ Zool 45: 1–91

    Google Scholar 

  • Lavette A (1969a) Sur la vêture schizophytique des flagellés symbiotes de termites. C R Acad Sci Paris Ser D 268: 2585–2587

    Google Scholar 

  • — (1969b) Les bactéries symbiotiques des flagellés termiticoles: cas deJoenia annectens. C R Acad Sci Paris Ser D 268: 1414–1416

    Google Scholar 

  • Lehninger AL (1985) Biochemie, 2nd edn. VCH, Weinheim

    Google Scholar 

  • Marshall KC (1991) The importance of studying microbial cell surfaces. In: Mozes N, Handley PS, Busscher HJ, Rouxhet PG (eds) Microbial cell surface analysis: structural and physicochemical methods. VCH, Weinheim, pp 3–19

    Google Scholar 

  • Matthysse AG (1992) Adhesion, bacterial. In: Lederberg J (eds) Encyclopedia of microbiology, vol 1. Academic Press, New York, pp 29–36

    Google Scholar 

  • Mozes N, Handley PS, Busscher HJ, Rouxhet PG (eds) (1991) Microbial cell surface analysis: structural and physicochemical methods. VCH, Weinheim

    Google Scholar 

  • Ofek I, Doyle RJ (eds) (1994) Bacterial adhesion to cells and tissues. Chapman and Hall, New York

    Google Scholar 

  • O'Brien RW, Slaytor M (1982) Role of microorganisms in the metabolism of termites. Aust J Biol Sci 35: 239–262

    Google Scholar 

  • Parker ND, Munn CB (1984) Increased cell surface hydrophobicity associated with possession of an additional surface protein byAeromonas salmonicida. FEMS Microbiol Lett 21: 233–237

    Google Scholar 

  • Radek R (1994)Monocercomonoides termitis n. sp., an oxymonad from the lower termiteKalotermes sinaicus. Arch Protistenk 144: 373–382

    Google Scholar 

  • —, Hausmann K, Breunig A (1992) Ectobiotic and endobiotic bacteria associated with the termite flagellateJoenia annectens. Acta Protozool 31: 93–107

    Google Scholar 

  • —, Rösel J, Hausmann K (1996) Light and electron microscopic study of the bacterial adhesion to termite flagellates applying lectin cytochemistry. Protoplasma 193: 105–122

    Google Scholar 

  • Rosenberg M, Rosenberg E, Judes H, Weiss E (1983) Bacterial adherens to hydrocarbons and to surfaces in the oral cavity. FEMS Microbiol Lett 20: 1–5

    Google Scholar 

  • Sleytr UB, Messner P (1988) Crystalline surface layers in prokaryotes. J Bacteriol 170: 2891–2897

    Google Scholar 

  • — —, Pum D (1988) Analysis of crystalline bacterial surface layers by freeze-etching, metal shadowing, negative staining and ultrathin sectioning. In: Mayer F (ed) Methods in microbiology, vol 20, electron microscopy in microbiology. Academic Press, London, pp 29–60

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Clin Microbiol Res 3: 197–218

    Google Scholar 

  • Talamás-Rohana P, Hernández-Ramirez VI, Perez-García JN, Ventura-Juárez J (1998)Entamoeba histolytica contains a β1 integrin-like molecule similar to fibronectin receptors from eukaryotic cells. J Euk Microbiol 45: 356–360

    Google Scholar 

  • Tamm SL (1980) The ultrastructure of prokaryotic-eukaryotic cell junctions. J Cell Sci 44: 335–352

    Google Scholar 

  • — (1982) Flagellated ectosymbiotic bacteria propel a eukaryotic cell. J Cell Biol 94: 697–709

    Google Scholar 

  • Vogels GD, Hoppe W, Stumm CK (1980) Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 40: 608–612

    Google Scholar 

  • Wadström T (1990) Hydrophobic characterization of staphylococci: role of surface structures and role in adhesion and host colonization. In: Doyle RJ, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, DC, pp 315–333

    Google Scholar 

  • Williams AG, Coleman GS (1992) The rumen protozoa. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Morphology and Ecology, Institute of Zoology, University of Heidelberg, Im Neuenheimer Feld 230, D-69120, Heidelberg, Germany

    R. Radek

  2. Institute of Plant Physiology and Microbiology, Free University of Berlin, Berlin

    G. Tischendorf

Authors
  1. R. Radek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Tischendorf
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Radek, R., Tischendorf, G. Bacterial adhesion to different termite flagellates: Ultrastructural and functional evidence for distinct molecular attachment modes. Protoplasma 207, 43–53 (1999). https://doi.org/10.1007/BF01294712

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01294712

Keywords

Search

Navigation