Journal of Industrial Microbiology

, Volume 17, Issue 3–4, pp 205–213 | Cite as

Phylogeny of mycolic acid-containing actinomycetes

  • J Chun
  • S-O Kang
  • Y C Hah
  • M Goodfellow


Almost-complete 16S rRNA sequences of 32 representatives of the generaCorynebacterium, Gordona, Mycobacterium, Nocardia, Rhodococcus, Tsukamurella andTuricella were examined using the neighbor-joining, Fitch-Margoliash, maximum parsimony and maximum likelihood methods in order to clarify the suprageneric relationships of these taxa. The topology of the resultant phylogenetic trees was only marginally affected by the use of the different algorithms. Several outgroup strains were used to try and establish the position of the root in the mycolata evolutionary tree. Most of the outgroup strains gave estimates of root positions that proved to be inconsistent when the different tree-making algorithms were used. However it was possible to assign the test strains to two suprageneric lineages the members of which can be distinguished using chemical markers. The familyCorynebacteriaceae encompasses the generaCorynebacterium, Dietzia andTuricella and the familyMycobacteriaceae, the generaGordona, Mycobacterium, Nocardia, Rhodococcus andTsukamurella. Nocardia pinensis formed a distinct clade that was most closely related to theGordona lineage. Emended descriptions are given of the two suprageneric taxa.


mycolata suprageneric classification rRNA sequencing chemotaxonomy 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Blackall LL, JH Parlett, AC Hayward, DE Minnikin, PF Greenfield and AE Harbers. 1989.Nocardia pinensis sp nov, an actinomycete found in activated sludge foams in Australia. J Gen Microbiol 135: 1547–1558.Google Scholar
  2. 2.
    Blackall LL, SC Barker and P Hugenholtz. 1994. Phylogenetic analysis and taxonomic history ofNocardia pinensis andNocardia amarae. Syst Appl Microbiol 17: 519–525.Google Scholar
  3. 3.
    Castellani A and AJ Chalmers. 1919. Manual of Tropical Medicine, 3rd edn. William, Wood and Co, New York.Google Scholar
  4. 4.
    Chester FD. 1987. Report of the mycologist: bacteriological work. Del Agric Exp Sta Bull 9: 38–145.Google Scholar
  5. 5.
    Chun J. 1995. Computer-Assised Classification and Identification of Actinomycetes. PhD Thesis, University of Newcastle upon Tyne, UK.Google Scholar
  6. 6.
    Chun J and M Goodfellow. 1995. A phylogenetic analysis of the genusNocardia with 16S rRNA gene sequences. Int J Syst Bacteriol 45: 240–245.PubMedGoogle Scholar
  7. 7.
    Collins MD and CS Cummins. 1986. GenusCorynebacterium Lehmann and Neumann 1896, 350Al. In: Bergey's Manual of Systematic Bacteriology, Vol 2 (Sneath PHA, NS Mair, ME Sharpe and JG Holt, eds), pp 1266–1276, Williams and Wilkins, Baltimore, MD.Google Scholar
  8. 8.
    Collins MD, J Smida, M Dorsch and E Stackebrandt. 1988.Tsukamurella gen nov harboringCorynebacterium paurometabolum andRhodococcus aurantiacus. Int J Syst Bacteriol 38: 385–391.Google Scholar
  9. 9.
    Collins MD, RA Burton and D Jones. 1988.Corynebacterium amycolatum sp nov. A new mycolic acid-lessCorynebacterium species from human skin. FEMS Microbiol Lett 49: 349–352.Google Scholar
  10. 10.
    Colwell RR. 1970. Polyphasic taxonomy in bacteria. In: Culture Collections of Microorganisms (Iizuka H and T Hasegawa, eds), pp 421–436, University of Tokyo, Tokyo.Google Scholar
  11. 11.
    De Queiroz K and J Gauthier. 1994. Toward a phylogenetic system of biological nomenclature. Trends Ecol Evol 9: 27–31.Google Scholar
  12. 12.
    Embley TM and E Stackebrandt. 1994. The molecular phylogeny and systematics of the actinomycetes. Ann Rev Microbiol 48: 257–289.Google Scholar
  13. 13.
    Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376.PubMedGoogle Scholar
  14. 14.
    Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.Google Scholar
  15. 15.
    Felsenstein J. 1993. PHYLIP (phylogenetic inference package) version 3.5c. Department of Genetics, University of Washington, Seattle, USA.Google Scholar
  16. 16.
    Fitch WM and E Margoliash. 1967. Construction of phylogenetic trees: a method based on mutation distances and estimated from cytochromec sequences is of general applicability. Science 155: 279–284.PubMedGoogle Scholar
  17. 17.
    Funke G, S Stubbs, M Altwegg, A Carlotti and MD Collins. 1994.Turicella otitidis gen nov, sp nov, a coryneform bacterium isolated from patients with otitis media. Int J Syst Bacteriol 44: 270–273.PubMedGoogle Scholar
  18. 18.
    Goodfellow M. 1971. Numerical taxonomy of some nocardioform bacteria. J Gen Microbiol 69: 33–80.PubMedGoogle Scholar
  19. 19.
    Goodfellow M. 1989. GenusRhodococcus Zopf 1891, 28AL. In: Bergey's Manual of Systematic Bacteriology, Vol 4 (Williams ST, ME Sharpe and JG Holt, eds), pp 2362–2371, Williams and Wilkins, Baltimore.Google Scholar
  20. 20.
    Goodfellow M. 1989. Suprageneric classification of actinomycetes. In: Bergey's Manual of Systematic Bacteriology, Vol 4 (Williams ST, ME Sharpe and JG Holt, eds), pp 2333–2339, Williams and Wilkins, Baltimore.Google Scholar
  21. 21.
    Goodfellow M. 1992. The familyNocardiaceae. In: The Prokaryotes, 2nd edn (Balows A, HG Trüper, M Dworkin, W Harder and KH Schleifer, eds), pp 1188–1213, Springer-Verlag, New York.Google Scholar
  22. 22.
    Goodfellow M and MP Lechevalier. 1989. The genusNocardia Trevisan 1889, 9AL. In: Bergey's Manual of Systematic Bacteriology, Vol 4 (Williams ST, ME Sharpe and JG Holt, eds), pp 2350–2361, Williams and Wilkins, Baltimore.Google Scholar
  23. 23.
    Goodfellow M and AG O'Donnell. 1994. Chemical Methods in Prokaryotic Systematics. John Wiley & Sons, Chichester.Google Scholar
  24. 24.
    Goodfellow M, A Lind, H Mordarska, S Pattyn and M Tsukamura. 1974. A co-operative numerical analysis of cultures considered to belong to the ‘rhodochrous’ taxon. J Gen Microbiol 85: 291–302.PubMedGoogle Scholar
  25. 25.
    Goodfellow M, J Chun, S Stubbs and AS Toboli. 1994. Transfer ofNocardia amarae Lechevalier and Lechevalier to the genusGordona asGordona amarae comb nov. Lett Appl Microbiol 19: 401–405.PubMedGoogle Scholar
  26. 26.
    Goodfellow M, R Davenport, FM Stainsby and TP Curtis. 1996. Actinomycete diversity associated with foaming in activated sludge plants. J Ind Microbiol 17: 268–280.Google Scholar
  27. 27.
    Goodfellow M, GP Manfio and J Chun. 1996. Towards a practical species concept for cultivable bacteria. In: Biodiversity: The Species in Practice (Claridge MF, HA Dawah and MR Wilson, eds), Chapman and Hall, Oxford.Google Scholar
  28. 28.
    Hennecke H, K Kaluza, B Thörsy, N Fuhrmann, W Ludwig and E Stackebrandt. 1985. Concurrent evolution of nitrogenase genes and 16S rRNA inRhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142: 342–348.Google Scholar
  29. 29.
    Herrera-Alcaraz EA, PL Valero-Guillèn, F Martin-Luengo and F Soriano. 1990. Taxonomic implications of the chemical analysis of the D2 group of corynebacteria. FEMS Microbiol Lett 73: 341–344.Google Scholar
  30. 30.
    Hillis DM, W Allard and MM Miyamoto. 1993. Analysis of DNA sequence data: phylogenetic inference. Meth Enzymol 224: 456–487.PubMedGoogle Scholar
  31. 31.
    Howarth OW, E Grund, RM Kroppenstedt and MD Collins. 1986. Structural determination of a new naturally occurring cyclic vitamin K. Biochem Biophys Res Commun 140: 916–923.PubMedGoogle Scholar
  32. 32.
    Jukes TH and CR Cantor. 1969. Evolution of protein molecules. In: Mammalian Protein Metabolism (Munro HN, ed), pp 21–132, Academic Press, New York.Google Scholar
  33. 33.
    Kim J. 1993. Improving the accuracy of phylogenetic estimation by combining different methods. Syst Biol 42: 331–340.Google Scholar
  34. 34.
    Klatte S, FA Rainey and RM Kroppenstedt. 1994. Transfer ofRhodococcus aichiensis Tsukamura 1982 andNocardia amarae Lechevalier and Lechevalier 1974 to the genusGordona asGordona aichiensis comb nov andGordona amarae comb nov. Int J Syst Bacteriol 44: 769–773.PubMedGoogle Scholar
  35. 35.
    Kluge AG and FS Farris. 1969. Quantitative phyletics and the evolution of anurans. Syst Zool 18: 1–32.Google Scholar
  36. 36.
    Larsen N, GJ Olsen, BL Maidak, MJ McCaughey, R Overbeek, TJ Macke, TL Marsh and CR Woese. 1993. The ribosomal database project. Nucleic Acids Res 21: 3021–3023.PubMedGoogle Scholar
  37. 37.
    Lechevalier HA and MP Lechevalier. 1970. A critical evaluation of the genera of aerobic actinomycetes. In: The Actinomycetales (Prauser H, ed), pp 393–405, Gustav Fischer Verlag, Jena.Google Scholar
  38. 38.
    Lehmann KB and R Neumann. 1896. Atlas und Grundriss der Bakteriologie und Lehrbuch der speciellen bakteriologischen Diagnostik, Teil II. JF Lehmann, München.Google Scholar
  39. 39.
    Lehmann KB and R Neumann. 1907. Lehmann's Medzin, Handatlanten. X. Atlas und und Grundriss der Bakteriologie und Lehrbuch der speciellan bakteriologischen Diagnostik, 4 Auflage. JF Lehmann, Munchen.Google Scholar
  40. 40.
    Ludwig W and KH Schleifer. 1994. Bacterial phylogeny based on 16S and 23S rRNA sequence analysis. FEMS Microbiol Lett 15: 155–173.Google Scholar
  41. 41.
    McNeil M and J Brown. 1994. The medically important actinomycetes: epidemiology and microbiology. Clin Microbiol Rev 7: 357–417.PubMedGoogle Scholar
  42. 42.
    Ochi K. 1995. Phylogenetic analysis of mycolic acid-containing wall-chemotype IV actinomycetes and allied taxa by partial sequencing of ribosomal protein AT-L30. Int J Syst Bacteriol 45: 653–660.PubMedGoogle Scholar
  43. 43.
    O'Donnell AG, TM Embley and M Goodfellow. 1993. Future of bacterial systematics. In: Handbook of New Bacterial Systematics (Goodfellow M and AG O'Donnell, eds), pp 513–524, Academic Press, London.Google Scholar
  44. 44.
    Olsen GJ, H Matsuda, R Hagstrom and R Overbeek. 1994. FastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comp Appl Biol Sci 10: 41–48.Google Scholar
  45. 45.
    Pankhurst RJ. 1995. Some problems in the methodology of cladistics. Binary 7: 37–41.Google Scholar
  46. 46.
    Pascual C, PA Lawson, JAE Farrow, MN Gimenez and MD Collins. 1995. Phylogenetic anlaysis of the genusCorynebacterium based on 16S rRNA gene sequences. Int J Syst Bacteriol 45: 724–728.PubMedGoogle Scholar
  47. 47.
    Pitcher D, A Soto, F Soriano and P Valero-Guillèn. 1992. Classification of coryneform bacteria associated with human urinary tract infection (group D2) asCorynebacterium urealyticum sp nov. Int J Syst Bacteriol 42: 178–181.PubMedGoogle Scholar
  48. 48.
    Pitulle C, M Dorsch, J Kazda, J Wolters and E Stackebrandt. 1992. Phylogeny of rapidly growing members of the genusMycobacterium. Int J Syst Bacteriol 42: 337–343.PubMedGoogle Scholar
  49. 49.
    Rainey FA, J Burghardt, RM Kroppenstedt, S Klatte and E Stackebrandt. 1995. Phylogenetic analysis of the generaRhodococcus andNocardia and evidence for the evolutionary origin of the genusNocardia from within the radiation ofRhodococcus species. Microbiology 141: 523–528.Google Scholar
  50. 50.
    Rainey FA, S Klatte, RM Kroppenstedt and E Stackebrandt. 1995.Dietzia, a new genus includingDietzia maris comb nov, formerlyRhodococcus maris. Int J Syst Bacteriol 45: 32–36.PubMedGoogle Scholar
  51. 51.
    Rogall T, J Wolters, T Flohr and EC Böttger. 1990. Towards a phylogeny and definition of species at the molecular level within the genusMycobacterium. Int J Syst Bacteriol 40: 323–330.PubMedGoogle Scholar
  52. 52.
    Ruimy R, P Boiron, V Boivin and R Christen. 1994. A phylogeny of the genusNocardia deduced from the analysis of small-subunit ribosomal DNA sequences, including transfer ofNocardia amarae to the genusGordona asGordona amarae comb nov. FEMS Microbiol Lett 123: 261–268.PubMedGoogle Scholar
  53. 53.
    Ruimy R, P Riegel, P Boiron, H Monteil and R Christen. 1995. Phylogeny of the genusCorynebacterium deduced from analyses of small-subunit ribosomal DNA sequences. Int J Syst Bacteriol 45: 740–746.PubMedGoogle Scholar
  54. 54.
    Saitou N and M Nei. 1987. The neighbor joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4: 406–425.PubMedGoogle Scholar
  55. 55.
    Schleifer KH and O Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407–477.PubMedGoogle Scholar
  56. 56.
    Schuppler M, F Mertens, G Schön and UB Göbel. 1995. Molecular characterisation of nocardioform actinomycetes in activated sludge by 16S rRNA analysis. Microbiology 141: 513–521.PubMedGoogle Scholar
  57. 57.
    Stackebrandt E, J Smida and MD Collins. 1988. Evidence of phylogenetic heterogeneity within the genusRhodococcus: revival of the genusGordona (Tsukamura). J Gen Appl Microbiol 34: 341–348.Google Scholar
  58. 58.
    Stahl DA and JW Urbance. 1990. The division between fast- and slow-growing species corresponds to natural relationships among the mycobacteria. J Bacteriol 172: 116–124.PubMedGoogle Scholar
  59. 59.
    Swofford DL and GJ Olsen. 1990. Phylogenetic reconstruction. In: Molecular Systematics (Hillis D and C Moritz, eds), pp 411–501, Sinauer Associates, Sunderland (USA).Google Scholar
  60. 60.
    Trevisan V. 1889. I Generi e la Specie dell Batteriacee. Zanaboni and Gabuzzi, Milano.Google Scholar
  61. 61.
    Tsukamura M. 1971. Proposal of a new genus,Gordona, for slightly acid-fast organisms occurring in sputa of patients with pulmonary disease and in soil. J Gen Microbiol 68: 15–26.PubMedGoogle Scholar
  62. 62.
    Tsukamura M. 1974. A further numerical taxonomic study of the rhodochrous group. Jap J Microbiol 18: 37–44.PubMedGoogle Scholar
  63. 63.
    Wayne LG and GP Kubica. 1986. GenusMycobacterium Lehmann and Neumann 1896, 363AL. In: Bergey's Manual of Systematic Bacteriology, Vol 2 (Sneath PHA, NS Mair, ME Sharpe and JG Holt, eds), pp 1436–1457, Williams and Wilkins, Baltimore.Google Scholar
  64. 64.
    Woese CR. 1987. Bacterial evolution. Microbiol Rev 51: 221–272.PubMedGoogle Scholar
  65. 65.
    Zopf W. 1891. Uber Ausscheidung von Fellfarbstoffen (Lipochromen) setens gewisser Spattpilze. Ber Deut Bot Ges 9: 22–28.Google Scholar

Copyright information

© Society for Industrial Microbiology 1996

Authors and Affiliations

  • J Chun
    • 1
  • S-O Kang
    • 1
  • Y C Hah
    • 1
  • M Goodfellow
    • 2
  1. 1.Department of Microbiology and Research Center for Molecular MicrobiologySeoul National UniversitySeoulRepublic of Korea
  2. 2.Department of MicrobiologyThe Medical SchoolNewcastle upon TyneUK

Personalised recommendations