Skip to main content
Log in

Numerical phenetic classification of clinically significant aerobic sporoactinomycetes and related organisms

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Clinically significant aerobic sporoactinomycetes, notably agents of mycetoma, were examined for a balanced set of unit characters and the resultant data analysed using standard numerical taxonomic procedures. All save two of the one hundred and seventy three tested strains were assigned to three multimembered cluster-groups, which encompassed sixteen major (4–7 strains), ten minor (2–3 strains) and forty single membered clusters, in an analysis based on the simple matching coefficient and unweighted pair group method with arithmetic averages algorithm. The three cluster-groups were equated with the genus Actinomadura (including Actinocorallia and Streptomyces somaliensis strains), and the genera Nocardiopsis and Streptomyces, and Thermobifida and Thermomonospora, respectively. In a corresponding principal co-ordinates analysis four multimembered groups corresponding to the genera Actinomadura, Nocardiopsis, Streptomyces, and Thermobifida and Thermomonospora were recognised. The causal agents of actinomycetoma were not only assigned to established taxa, notably, to Actinomadura latina, Actinomadura madurae, Actinomadura pelletieri and Streptomyces somaliensis, but also to additional centres of taxonomic variation which were equated with the rank of species. Most of the streptomycetes isolated from clinical material were assigned to clusters equated with the species Streptomyces albus and Streptomyces anulatus. The numerical taxonomic data were used to generate a frequency matrix designed to facilitate the identification of clinically significant Actinomadura, Nocardiopsis and Streptomyces strains to the species level; rapid enzyme tests accounted for eleven out of the twenty-one diagnostic tests.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alderson G. 1985. The application and relevance of non-hierarchic methods in bacterial taxonomy. In: Goodfellow M., Jones D. and Priest F.G. (eds), Computer-Assisted Bacterial Systematics. Academic Press, London, pp. 227–273.

    Google Scholar 

  • Alderson G. and Goodfellow M. 1979. Classification and identification of actinomycetes causing mycetoma. Post. Hig. I Med. Dósw 44: 109–124.

    Google Scholar 

  • Alderson G., Athalye M. and White R.P. 1984. Numerical methods in the taxonomy of sporoactinomycetes. In: Ortiz-Ortiz L., Bojalil L.F. and Yakoleff V. (eds), Biological, Biochemical and Biomedical Aspects of Actinomycetes. Academic Press, London, pp. 597–615.

    Google Scholar 

  • Atalan E., Manfio G.P., Ward A.C., Kroppenstedt R.M. and Goodfellow M. 2000. Biosystematic studies on novel streptomycetes from soil. Antonie van Leeuwenhoek 77: 337–353.

    Article  PubMed  CAS  Google Scholar 

  • Athalye M., Lacey J. and Goodfellow M. 1981. Selective isolation and enumeration of actinomycetes using rifampicin. J. appl. Bact 51: 289–297.

    CAS  Google Scholar 

  • Athalye M., Goodfellow M., Lacey J. and White R.P. 1985. Numerical classification of Actinomadura and Nocardiopsis. Int. J. Syst. Bacteriol. 35: 86–98.

    Google Scholar 

  • Baril L., Boiron P., Manceron V., Ely S.O.O., Jamet P., Favre E. et al. 1999. Refractory craniofacial actinomycetoma due to Streptomyces somaliensis that required salvage therapy with amikacin and imipenem. Clin. Infect. Dis. 29: 460–461.

    Article  PubMed  CAS  Google Scholar 

  • Berd D. 1973. Laboratory identification of clinically important aerobic actinomycetes. Appl. Microbiol. 25: 665–681.

    PubMed  CAS  Google Scholar 

  • Develoux M., Dieng M.T. and Ndiaye B. 1999. Mycetoma. J. Mycol. Med. 9: 179–209.

    Google Scholar 

  • Elzein S., Quintana E.T., Hamid M.E., Maldonado L.A., Ahmed A.O., Kim B. et al. 2001. Characterisation of streptomycetes that cause mycetoma Abstracts of the 12th International Symposium on the Biology of Actinomycetes. The University of British Columbia, Vancouver, Canada, pp. 103.

    Google Scholar 

  • Evtushenko L.I., Taran V.V., Akimov V.N., Kroppenstedt R.M., Tiedje J.M. and Stackebrandt E. 2000. Nocardiopsis tropica sp. nov., nom. rev. and Nocardiopsis dassonvillei subsp albirubida subsp. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 50: 73–81.

    PubMed  CAS  Google Scholar 

  • Fischer A., Kroppenstedt R.M. and Stackebrandt E. 1983. Molecular-genetic and chemotaxonomic studies on Actinomadura and Nocardiopsis. J. Gen. Microbiol. 129: 3433–3446.

    PubMed  CAS  Google Scholar 

  • Goodfellow M. 1996. Actinomycetes: Actinomyces, Actinomadura, Nocardia, Streptomyces and related taxa. In: Collee J.G., Fraser A.G., Marmion B.P. and Simmons A. (eds), Mackie and McCartney Practical Medical Microbiology. Churchill Livingstone, Edinburgh, pp. 343–359.

    Google Scholar 

  • Goodfellow M. 1998. Nocardia and related genera. In: Balows A. and Duerden B.I. (eds), Topley Wilson's Microbiology and Microbial Infections. Systematic Bacteriology Vol. 2. 9th edn. Arnold, London, pp. 463–489.

  • Goodfellow M. and Pirouz T. 1982. Numerical classification of sporoactinomycetes containing meso-diaminopimelic acid in the cell wall. J. Gen. Microbiol. 128: 503–527.

    PubMed  CAS  Google Scholar 

  • Goodfellow M., Alderson G. and Lacey J. 1979. Numerical taxonomy of Actinomadura and related actinomycetes. J. Gen. Microbiol. 112: 95–111.

    PubMed  CAS  Google Scholar 

  • Goodfellow M., Weaver C.R. and Minnikin D.E. 1982. Numerical classification of rhodococci, corynebacteria and related organisms. J. Gen. Microbiol. 128: 731–745.

    PubMed  CAS  Google Scholar 

  • Goodfellow M., Embley T.M. and Austin B. 1985. Numerical taxonomy and emended description of Renibacterium salmoninarum. J. Gen. Microbiol. 131: 2739–2752.

    Google Scholar 

  • Goodfellow M., Lonsdale C., James A.L. and MacNamara O.C. 1987. Rapid biochemical tests for the characterisation of streptomycetes. FEMS Microbiol. Lett. 43: 39–44.

    Article  CAS  Google Scholar 

  • Goodfellow M., Stanton L.J., Simpson K.E. and Minnikin D.E. 1990. Numerical and chemical classification of Actinoplanes and some related actinomycetes. J. Gen. Microbiol. 136: 19–36.

    Google Scholar 

  • Goodfellow M., Trujillo M.E. and Alderson G. 1995. Approaches towards the identification of sporoactinomycetes that cause mycetoma. Biotechnologia 7-8: 271–286.

    Google Scholar 

  • Gordon R.E. 1976. A taxonomist's obligation. In: Goodfellow M., Brownell G.H. and Serrano J.A. (eds), The Biology of the Nocardiae. Academic Press, London, pp. 66–73.

    Google Scholar 

  • Grund E. and Kroppenstedt R.M. 1990. Chemotaxonomy and numerical taxonomy of the genus Nocardiopsis Meyer 1976. Int. J. Syst. Bacteriol. 40: 5–11.

    Google Scholar 

  • Hamid M.E., Chun J., Magee J.G., Minnikin D.E. and Goodfellow M. 1994. Rapid characterization and identification of mycobacteria using fluorogenic enzyme tests. Zbl. Bakt. 280: 433–438.

    Google Scholar 

  • Jones K.L. 1949. Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J. Bacteriol. 57: 141–146.

    PubMed  CAS  Google Scholar 

  • Kim B., Sahin N., Minnikin D.E., Zakrzewska-Czerwinska J., Mordarski M. and Goodfellow M. 1999. Classification of thermophilic streptomycetes including the description of Streptomyces thermoalcalitolerans sp. nov. Int. J. Syst. Bacteriol. 49: 7–17.

    PubMed  Google Scholar 

  • Kroppenstedt R.M. 1992. The genus Nocardiopsis. In: Balows A., Trüper H.G., Dworkin W., Harder W. and Schleifer K.H. (eds), The Prokaryotes. 2nd edn. SpringerVerlag, New York, pp. 1139–1156.

    Google Scholar 

  • Kroppenstedt R.M., Stackebrandt E. and Goodfellow M. 1990. Taxonomic revision of the actinomycete genera Actinomadura and Micromonospora. Syst. Appl. Microbiol. 13: 148–160.

    CAS  Google Scholar 

  • Labeda D.P. 2001. Crossiella gen. nov., a new genus related to Streptoalloteicus. Int. J. Syst. Evol. Microbiol. 51: 1575–1579.

    PubMed  CAS  Google Scholar 

  • Langham C.D., Williams S.T., Sneath P.H.A. and Mortimer A.M. 1989. New probability matrices for identification of Streptomyces. J. Gen. Microbiol. 135: 121–133.

    PubMed  CAS  Google Scholar 

  • Lu Z., Wang L., Zhang Y., Shi Y., Liu Z., Quintana E.T. et al. 2003. Two new species of Actinomadura:Actinomadura catellatospora sp. nov. andActinomadura glaucoflava. Int. J. Syst. Microbiol. (in press).

  • Manfio G.P., Zakrzewska-Czerwinska J., Atalan E. and Goodfellow M. 1995. Towards minimal standards for the description of-Streptomyces species. Biotechnologia 7-8: 242–253.

    Google Scholar 

  • McCarthy A.J. and Cross T. 1984. A taxonomic study of Thermomonospora and other monosporic actinomycetes. J. Gen Microbiol. 130: 5–15.

    Google Scholar 

  • McNeil M.M., Brown J.M., Jarvis W.R. and Ajello O.L. 1990. Comparisons of species distribution and antimicrobial susceptibility of aerobic actinomycetes from clinical specimens. Rev. Infect. Dis. 12: 778–783.

    PubMed  CAS  Google Scholar 

  • McNeil M.M. and Brown J.M. 1994. The medically important aerobic actinomycetes epidemiology and microbiology. Clin. Microbiol. Rev. 7: 357–417.

    PubMed  CAS  Google Scholar 

  • McNeil M.M., Brown J.M., Scalise G. and Piersimoni C. 1992. Nonmycetomic Actinomadura madurae infection in a patient with AIDS. J. Clin. Microbiol. 30: 1008–1010.

    PubMed  CAS  Google Scholar 

  • Meyer J. 1976. Nocardiopsis; a new genus of the order Actinomycetales. Int. J. Syst. Bacteriol. 26: 487–493.

    Google Scholar 

  • Meyer J. 1989. Genus Actinomadura Lechevalier and Lechevalier 1970a, 400AL. In: Williams S.T., Sharpe M.E. and Holt J.G. (eds), Bergey's Manual of Systematic Bacteriology Vol. 4. Williams Wilkins, Baltimore, pp. 2511–2526.

    Google Scholar 

  • Mishra S.K., Gordon R.E. and Barnett D.A. 1980. Identification of nocardiae and streptomycetes of medical importance. J. Clin. Microbiol. 728–736.

  • Ndiaye B., Develoux M., Dieng M.T., Kane A., Ndir O. and Raphenon G. 2000. Actual presentation of mycetoma situation in Senegal. J. Mycol. Med. 10: 140–144.

    Google Scholar 

  • Ochi K.S., Miyadoh S. and Tamura T. 1991. Polyacrylamide gel electrophoresis analysis of ribosomal protein At-L30 as a novel approach to actinomycete taxonomy: application to the genera Actinomadura and Microtetraspora. Int. J. Syst. Bacteriol. 41: 234–239.

    PubMed  CAS  Google Scholar 

  • O'Donnell A.G., Falconer C., Goodfellow M., Ward A.C. and Williams E. 1993. Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie van Leeuwenhoek 64: 325–340.

    Article  PubMed  Google Scholar 

  • Poschner J., Kroppenstedt R.M., Fischer A. and Stackebrandt E. 1985. DNA:DNA reassociation and chemosystematic studies on Actinomadura, Microbispora, Microtetraspora, Micropolyspora and Nocardiopsis. System. Appl. Microbiol. 6: 264–270.

    CAS  Google Scholar 

  • Rainey F.A., Ward-Rainey N., Kroppenstedt R.M. and Stackebrandt E. 1996. The genus Nocardiopsis represents a phylogenetically coherent and a distinct actinomycete lineage: Proposal of Nocardiopsaceae fam nov. Int. J. Syst. Bacteriol. 46: 1088–1092.

    PubMed  CAS  Google Scholar 

  • Schaal K.P. 1985. Laboratory diagnosis of actinomycete diseases. In: Goodfellow M. and Minnikin D.E. (eds), Chemical Methods in Bacterial Systematics. Academic Press, London, pp. 359–381.

    Google Scholar 

  • Schaal K.P. and Beaman B.L. 1984. Clinically significant actinomycetes. In: Goodfellow M., Mordarski M. and Williams S.T. (eds), The Biology of the Actinomycetes. Academic Press, London, pp. 389–424.

    Google Scholar 

  • Schaal K.P. and Lee H.-J. 1992. Actinomycete infections in humans-a review. Gene 115: 201–211.

    Article  PubMed  CAS  Google Scholar 

  • Sindhuphak W.E., MacDonald E. and Head E. 1985. Actinomycetoma caused by Nocardiopsis dassonvillei. Arch. Dermatol. 121: 1332–1334.

    Article  PubMed  CAS  Google Scholar 

  • Silvestri L.G., Turri M., Hill L.R. and Gilardi D. 1962. A quantitative approach to systematics of actinomycetes based on overall similarity. In: Ainsworth G.C. and Sneath P.H.A. (eds), Microbial Classification. Cambridge University Press, Cambridge, pp. 333–360.

    Google Scholar 

  • Sneath P.H.A. 1957. Some thoughts on bacterial classification. J. Gen. Microbiol. 17: 184–200.

    PubMed  CAS  Google Scholar 

  • Sneath P.H.A. 1978. Classification of micro-organisms. In: Norris J.R. and Richmond M.H. (eds), Essays in Microbiology. John Wiley Sons, Chichester, pp. 1–31.

    Google Scholar 

  • Sneath P.H.A. 1979a. BASIC program for identification of an unknown with presence-absence data against an identification matrix of percent positive characters. Comp. Geosci. 5: 195–213.

    Article  Google Scholar 

  • Sneath P.H.A. 1979b. BASIC program for character separation indices from an identification matrix of percent positive characters. Comp. Geosci. 5: 349–357.

    Article  Google Scholar 

  • Sneath P.H.A. 1980a. BASIC program for the most diagnostic properties of groups from an identification matrix of percent positive characters. Comp. Geosci. 6: 21–26.

    Article  Google Scholar 

  • Sneath P.H.A. 1980b. BASIC program for determining the best identification scores possible for the most typical example when compared with an identification matrix of percent positive characters. Comp. Geosci. 6: 27–34.

    Article  Google Scholar 

  • Sneath P.H.A. 1980c. BASIC program for determining overlap between groups in an identification matrix of percent positive characters. Comp. Geosci. 6: 267–278.

    Article  Google Scholar 

  • Sneath P.H.A. and Johnson R. 1972. The influence on numerical taxonomic similarities of errors in microbiological tests. J. Gen. Microbiol. 72: 377–392.

    PubMed  CAS  Google Scholar 

  • Sneath P.H.A. and Sokal R.R. 1973. Numerical Taxonomy. The Principles and Practice of Numerical Classification. W.H. Freeman, Baltimore.

    Google Scholar 

  • Society for Actinomycetes Japan 2001. Identification Manual of Actinomycetes. Business Centre for Academic Societies, Tokyo, Japan.

    Google Scholar 

  • Sokal R.R. and Michener C.D. 1958. A statistical method for evaluating systematic relationships. Kans. Univ. Sci. Bull. 38: 1409–1438.

    Google Scholar 

  • Sokal R.R. and Rohlf F.J. 1962. The comparison of dendrograms by objective methods. Taxon XI 33–40.

  • Stackebrandt E., Rainey F.A. and Ward-Rainey N.-L. 1997. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int. J. Syst. Bacteriol. 47: 479–491.

    Article  Google Scholar 

  • Staneck J.L. and Roberts G.D. 1974. Simplified approach to identification of aerobic actinomycetes by thin layer chromatography. Appl. Microbiol. 28: 226–231.

    PubMed  CAS  Google Scholar 

  • Trujillo M.E. and Goodfellow M. 1997. Polyphasic taxonomic study of clinically significant actinomadurae including the description of Actinomadura latina sp. nov. Zbl. Bakt. 285: 212–233.

    CAS  Google Scholar 

  • Whitham T.S., Athalye M., Minnikin D.E. and Goodfellow M. 1993. Numerical and chemical classification of Streptosporangium and some related taxa. Antonie van Leeuwenhoek 64: 387–429.

    Article  PubMed  Google Scholar 

  • Wilkinson B.J. and Jones D. 1977. A numerical taxonomic survey of Listeria and related bacteria. J. Gen. Microbiol. 77: 317–330.

    Google Scholar 

  • Williams S.T., Goodfellow M., Wellington E.M.H., Vickers J.C., Alderson G., Sneath P.H.A. et al. 1983. A probability matrix for identification of some streptomycetes. J. Gen. Microbiol 129: 1815–1830.

    PubMed  CAS  Google Scholar 

  • Williams S.T., Goodfellow M. and Alderson G. 1989. Genus Streptomyces Waksman and Henrici 1943, 339AL. In: Williams S.T., Sharpe M.E. and Holt J.G. (eds), Bergey's Manual of Systematic Bacteriology Vol. 4. Williams and Wilkins, Baltimore, pp. 2452–2492.

    Google Scholar 

  • Wishart D. 1978. Clustan User Manual,Version IC, Release 2. 3rd edn. Edinburgh University Program Library Unit, Edinburgh.

    Google Scholar 

  • Wust J., Lanzendorfer H., von Graevenitz A., Gloer H.J. and Schmid B. 1990. Peritonitis caused by Actinomadura madurae in a patent on CAPD. Eur. J. Clin. Microbiol. Infect. Dis. 9: 700–701.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Zhang Z., Kudo T., NakayimaY. and Wang Y. 2001. Clarification of the relationship between the members of the family Thermomonosporaceae on the basis of 16S rDNA, 16S-23S rRNA internal transcribed spacer and 23S rDNA sequences and chemotaxonomic analyses. Int. J. Syst. Evol. Microbiol. 51: 373–383.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Goodfellow.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trujillo, M.E., Goodfellow, M. Numerical phenetic classification of clinically significant aerobic sporoactinomycetes and related organisms. Antonie Van Leeuwenhoek 84, 39–68 (2003). https://doi.org/10.1023/A:1024401004258

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024401004258

Navigation