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. 1979 Dec;26(3):1146–1158. doi: 10.1128/iai.26.3.1146-1158.1979

Ultrastructure of gliding bacteria: scanning electron microscopy of Capnocytophaga sputigena, Capnocytophaga gingivalis, and Capnocytophaga ochracea.

T P Poirier, S J Tonelli, S C Holt
PMCID: PMC414740  PMID: 528052

Abstract

When examined by both light and scanning electron microscopy, Capnocytophaga gingivalis, C. sputigena, and C. ochracea displayed three distinct growth zones: the original streak, an intermediate zone, and the advancing edge, or halo zone. On Trypticase (BBL Microbiology Systems)-soy-blood agar, the cells translocated by gliding. C. gingivalis and C. sputigena formed large, irregular isolated colonies, while C. ochracea formed a more confluent cell mass. The cells within the streak zone and in most of the intermediate zone were heaped into mounds, with the individual cells displaying a definite flow pattern, the latter characteristic of C. sputigena and C. gingivalis. The halo zone consisted of tracks of cells which appeared to have translocated back upon themselves, or were restricted in their outward movements by adjacent cells. Also present within the halo zone were small aggregates of cells, referred to as pioneer colonies. The cell surfaces of C. gingivalis and C. ochracea were smooth and free of any apparent extracellular material, whereas C. sputigena was covered with a thick amorphous material, as well as long, thick, cell surface-associated fibrils.

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Selected References

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  1. ANDERSON R. L., ORDAL E. J. Cytophaga succinicans sp. n., a factaltatively anaerobic, aquatic myxobacterium. J Bacteriol. 1961 Jan;81:130–138. doi: 10.1128/jb.81.1.130-138.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burchard R. P. Gliding motility mutants of Myxococcus xanthus. J Bacteriol. 1970 Nov;104(2):940–947. doi: 10.1128/jb.104.2.940-947.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Campos J. M., Zusman D. R. Regulation of development in Myxococcus xanthus: effect of 3':5'-cyclic AMP, ADP, and nutrition. Proc Natl Acad Sci U S A. 1975 Feb;72(2):518–522. doi: 10.1073/pnas.72.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cisar J. O., Vatter A. E., McIntire F. C. Identification of the virulence-associated antigen on the surface fibrils of Actinomyces viscosus T14. Infect Immun. 1978 Jan;19(1):312–319. doi: 10.1128/iai.19.1.312-319.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Edén C. S., Hanson L. A., Jodal U., Lindberg U., Akerlund A. S. Variable adherence to normal human urinary-tract epithelial cells of Escherichia coli strains associated with various forms of urinary-tract infection. Lancet. 1976 Sep 4;1(7984):490–492. [PubMed] [Google Scholar]
  6. FAUST L., WOLFE R. S. Enrichment and cultivation of Beggiatoa alba. J Bacteriol. 1961 Jan;81:99–106. doi: 10.1128/jb.81.1.99-106.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fowler J. E., Jr, Stamey T. A. Studies of introital colonization in women with recurrent urinary infections. VII. The role of bacterial adherence. J Urol. 1977 Apr;117(4):472–476. doi: 10.1016/s0022-5347(17)58501-8. [DOI] [PubMed] [Google Scholar]
  8. Freedman H. L., Listgarten M. A., Taichman N. S. Electron microscopic features of chronically inflamed human gingiva. J Periodontal Res. 1968;3(4):313–327. doi: 10.1111/j.1600-0765.1968.tb01937.x. [DOI] [PubMed] [Google Scholar]
  9. Freter R. Parameters affecting the association of vibrios with the intestinal surface in experimental cholera. Infect Immun. 1972 Aug;6(2):134–141. doi: 10.1128/iai.6.2.134-141.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gibbons R. J., Houte J. V. Bacterial adherence in oral microbial ecology. Annu Rev Microbiol. 1975;29:19–44. doi: 10.1146/annurev.mi.29.100175.000315. [DOI] [PubMed] [Google Scholar]
  11. Grilione P. L., Pangborn J. Scanning electron microscopy of fruiting body formation by myxobacteria. J Bacteriol. 1975 Dec;124(3):1558–1565. doi: 10.1128/jb.124.3.1558-1565.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HAGEAGE G. J., Jr, MURRAY R. G. Random rotation among Vitreoscilla species. J Bacteriol. 1962 Dec;84:1345–1346. doi: 10.1128/jb.84.6.1345-1346.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Henrichsen J. Bacterial surface translocation: a survey and a classification. Bacteriol Rev. 1972 Dec;36(4):478–503. doi: 10.1128/br.36.4.478-503.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hohmann A., Wilson M. R. Adherence of enteropathogenic Escherichia coli to intestinal epithelium in vivo. Infect Immun. 1975 Oct;12(4):866–880. doi: 10.1128/iai.12.4.866-880.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holt S. C. Anatomy and chemistry of spirochetes. Microbiol Rev. 1978 Mar;42(1):114–160. doi: 10.1128/mr.42.1.114-160.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ingham H. R., Sisson P. R., Tharagonnet D., Selkon J. B., Codd A. A. Inhibition of phagocytosis in vitro by obligate anaerobes. Lancet. 1977 Dec 17;2(8051):1252–1254. doi: 10.1016/s0140-6736(77)92662-9. [DOI] [PubMed] [Google Scholar]
  17. Irving J. T., Socransky S. S., Tanner A. C. Histological changes in experimental periodontal disease in rats monoinfected with gram-negative organisms. J Periodontal Res. 1978 Jul;13(4):326–332. doi: 10.1111/j.1600-0765.1978.tb00187.x. [DOI] [PubMed] [Google Scholar]
  18. Jackson S. W., Zey P. N. Ultrastructure of lipopolysaccharide isolated from Treponema pallidum. J Bacteriol. 1973 May;114(2):838–844. doi: 10.1128/jb.114.2.838-844.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaufman E. J., Mashimo P. A., Hausmann E., Hanks C. T., Ellison S. A. Fusobacterial infection: enhancement by cell free extracts of Bacteroides melaninogenicus possessing collagenolytic activity. Arch Oral Biol. 1972 Mar;17(3):577–580. doi: 10.1016/0003-9969(72)90073-8. [DOI] [PubMed] [Google Scholar]
  20. Leadbetter E. R., Holt S. C., Socransky S. S. Capnocytophaga: new genus of gram-negative gliding bacteria. I. General characteristics, taxonomic considerations and significance. Arch Microbiol. 1979 Jul;122(1):9–16. doi: 10.1007/BF00408040. [DOI] [PubMed] [Google Scholar]
  21. Lopes J., Inniss W. E. Electron microscopic study of lipopolysaccharide from an avian strain of Escherichia coli O18. J Bacteriol. 1970 Jul;103(1):238–243. doi: 10.1128/jb.103.1.238-243.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Muse K. E., Collier A. M., Baseman J. B. Scanning electron microscopic study of hamster tracheal organ cultures infected with Bordetella pertussis. J Infect Dis. 1977 Dec;136(6):768–777. doi: 10.1093/infdis/136.6.768. [DOI] [PubMed] [Google Scholar]
  23. Newman M. G., Socransky S. S. Predominant cultivable microbiota in periodontosis. J Periodontal Res. 1977 Mar;12(2):120–128. doi: 10.1111/j.1600-0765.1977.tb00114.x. [DOI] [PubMed] [Google Scholar]
  24. Nitzan D., Sperry J. F., Wilkins T. D. Fibrinolytic activity of oral anaerobic bacteria. Arch Oral Biol. 1978;23(6):465–470. doi: 10.1016/0003-9969(78)90078-x. [DOI] [PubMed] [Google Scholar]
  25. Page R. C., Schroeder H. E. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest. 1976 Mar;34(3):235–249. [PubMed] [Google Scholar]
  26. Pangborn J., Kuhn D. A., Woods J. R. Dorsal-ventral differentiation in Simonsiella and other aspects of its morphology and ultrastructure. Arch Microbiol. 1977 Jun 20;113(3):197–204. doi: 10.1007/BF00492025. [DOI] [PubMed] [Google Scholar]
  27. ROSEBURY T., CLARK A. R., ENGEL S. G., TERGIS F. Studies of fusospirochetal infection. I. Pathogenicity for guinea pigs of individual and combined cultures of spirochetes and other anaerobic bacteria derived from the human mouth. J Infect Dis. 1950 Nov-Dec;87(3):217–225. doi: 10.1093/infdis/87.3.217. [DOI] [PubMed] [Google Scholar]
  28. SOCRANSKY S. S., GIBBONS R. J. REQUIRED ROLE OF BACTEROIDES MELANINOGENICUS IN MIXED ANAEROBIC INFECTIONS. J Infect Dis. 1965 Jun;115:247–253. doi: 10.1093/infdis/115.3.247. [DOI] [PubMed] [Google Scholar]
  29. Savage D. C., Blumershine R. V. Surface-surface associations in microbial communities populating epithelial habitats in the murine gastrointestinal ecosystem: scanning electron microscopy. Infect Immun. 1974 Jul;10(1):240–250. doi: 10.1128/iai.10.1.240-250.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Selinger D. S., Reed W. P. Pneumococcal adherence to human epithelial cells. Infect Immun. 1979 Feb;23(2):545–548. doi: 10.1128/iai.23.2.545-548.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shimkets L., Seale T. W. Fruiting-body formation and myxospore differentiation and germination in Mxyococcus xanthus viewed by scanning electron microscopy. J Bacteriol. 1975 Feb;121(2):711–720. doi: 10.1128/jb.121.2.711-720.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Socransky S. S., Holt S. C., Leadbetter E. R., Tanner A. C., Savitt E., Hammond B. F. Capnocytophaga: new genus of gram-negative gliding bacteria. III. Physiological characterization. Arch Microbiol. 1979 Jul;122(1):29–33. doi: 10.1007/BF00408042. [DOI] [PubMed] [Google Scholar]
  33. Socransky S. S. Microbiology of periodontal disease -- present status and future considerations. J Periodontol. 1977 Sep;48(9):497–504. doi: 10.1902/jop.1977.48.9.497. [DOI] [PubMed] [Google Scholar]
  34. Stanier R. Y. Studies on Nonfruiting Myxobacteria: I. Cytophaga johnsonae, n.sp., a Chitin-decomposing Myxobacterium. J Bacteriol. 1947 Mar;53(3):297–315. [PMC free article] [PubMed] [Google Scholar]
  35. Stanier R. Y. Studies on the Cytophagas. J Bacteriol. 1940 Nov;40(5):619–635. doi: 10.1128/jb.40.5.619-635.1940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sutherland I. W. Bacterial exopolysaccharides. Adv Microb Physiol. 1972;8:143–213. doi: 10.1016/s0065-2911(08)60190-3. [DOI] [PubMed] [Google Scholar]
  37. Takeuchi H., Sumitani M., Tsubakimoto K., Tsutsui M. Oral microorganisms in the gingiva of individuals with periodontal disease. J Dent Res. 1974 Jan-Feb;53(1):132–136. doi: 10.1177/00220345740530010601. [DOI] [PubMed] [Google Scholar]
  38. Voelz H., Reichenbach H. Fine structure of fruiting bodies of Stigmatella aurantiaca (Myxobacterales). J Bacteriol. 1969 Sep;99(3):856–866. doi: 10.1128/jb.99.3.856-866.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ward M. E., Watt P. J. Adherence of Neisseria gonorrhoeae to urethral mucosal cells: an electron-microscopic study of human gonorrhea. J Infect Dis. 1972 Dec;126(6):601–605. doi: 10.1093/infdis/126.6.601. [DOI] [PubMed] [Google Scholar]
  40. Woo D. D., Holt S. C., Leadbetter E. R. Ultrastructure of Bacteroides species: Bacteroides asaccharolyticus, Bacteroides fragilis, Bacteroides melaninogenicus subspecies melaninogenicus, and B. melaninogenicus subspecies intermedius. J Infect Dis. 1979 May;139(5):534–546. doi: 10.1093/infdis/139.5.534. [DOI] [PubMed] [Google Scholar]

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